The Socioecology, Mating System and Behavior of Round- Tailed Ground Squirrels (Xerospermophilus tereticaudus)
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Authors Munroe, Karen Elizabeth
Publisher The University of Arizona.
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THE SOCIOECOLOGY, MATING SYSTEM AND BEHAVIOR OF ROUND-TAILED GROUND SQUIRRELS (XEROSPERMOPHILUS TERETICAUDUS)
by
Karen Elizabeth Munroe
______
A Dissertation Submitted to the Faculty of the
THE SCHOOL OF NATURAL RESOURCES AND THE ENVIRONMENT
In Partial Fulfillment of the Requirements For the Degree of
DOCTOR OF PHILOSOPHY WITH A MAJOR IN WILDLIFE AND FISHERIES SCIENCE
In the Graduate College
THE UNIVERSITY OF ARIZONA
2011
2
THE UNIVERSITY OF ARIZONA GRADUATE COLLEGE
As members of the Dissertation Committee, we certify that we have read the dissertation
prepared by Karen E. Munroe
entitled: The socioecology, mating system and behavior of round-tailed ground squirrels (Xerospermophilus tereticaudus)
and recommend that it be accepted as fulfilling the dissertation requirement for the
Degree of Doctor of Philosophy
______Date: 9 May 2011 John L. Koprowski
______Date: 9 May 2011 William J. Matter
______Date: 9 May 2011 Guy. R McPherson
______Date: 9 May 2011 Robert J. Steidl
Final approval and acceptance of this dissertation is contingent upon the candidate’s submission of the final copies of the dissertation to the Graduate College.
I hereby certify that I have read this dissertation prepared under my direction and recommend that it be accepted as fulfilling the dissertation requirement.
______Date: 9 May 2011 Dissertation Director: John L. Koprowski
3
STATEMENT BY AUTHOR
This dissertation has been submitted in partial fulfillment of requirements for an advanced degree at the University of Arizona and is deposited in the University Library to be made available to borrowers under rules of the Library.
Brief quotations from this dissertation are allowable without special permission, provided that accurate acknowledgment of source is made. Requests for permission for extended quotation from or reproduction of this manuscript in whole or in part may be granted by the head of the major department or the Dean of the Graduate College when in his or her judgment the proposed use of the material is in the interests of scholarship. In all other instances, however, permission must be obtained from the author.
SIGNED: Karen E. Munroe
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ACKNOWLEDGMENTS
I am deeply indebted and grateful for many people who have fortified, encouraged, promoted, bolstered and inspired me along this extensive journey. I wish to thank Dr. Michael Steele for becoming my undergraduate advisor, taking me under his wing, teaching me to question assumptions, showing me what science was all about (acorns and squirrels, of course!), and continuing to be a source of inspiration; Dr. Morris Levy for taking me into his lab, his home and his heart, serving as a mentor, advisor and a continual supporter with an eloquence and humor that only he could; Maria Mercedes Maya Levy for teaching me all the genetic techniques I know with grace, elegance and an artistic flair! I am immensely grateful to John Koprowski for serving as my major advisor, for pushing me to do my best, having patience with me as I learn, opening doors to amazing opportunities that will serve me well into my career, seeing my potential when I couldn’t. Although I hope to follow in his footsteps, I doubt I’ll ever be able to fill his shoes!! I also wish to thank my dissertation committee William Matter, Guy McPherson and Robert Steidl (and William Birky), whose generous support and guidance was always provided expediently and with appropriate sarcastic wit. Funding for this project was provided by the Western National Parks Association, T&E Incorporation Conservation Biology Research Grant, American Society of Mammalogists Grants-in-Aid Award, the Wildlife Foundation Scholarship, Sigma Xi Grant-in-Aid of Research, and the Alton A. Lindsey Award and Grant. The staff and volunteers of the Casa Grande Ruins National Monument not only made this project possible but made me part of their family and made every day in the field interesting and full of surprises. I am so grateful for my friends for providing assistance, support, and nourishment both scientifically and personally: Adam Boyko, Joseph Busch, Cori Carveth, Carina Eizmendi, Jessica Gwinn, Sara Jensen-O’Brien, Jim Kellam, Maureen McColgin, Cathy Mossman, Adrian Munguia-Vega, Monica Munoz-Torrez, Kerry Nicholson, Karla Pelz-Serrano, Lon Porter, Nancy Regens, Jay Turner, Cora Varas-Nelson, Tamara Wilson, and Carolina Yaber-Tenjo. I am indebted to and inspired by the entire Koprowski lab including: Seafha Blount, Debbie Buecher, Hsiang Ling Chen, Nichole Cudworth, Jonathan Derbridge, Sandy Doumas, Andrew Edelman, R. Nathan Gwinn, Vicki Greer, Sarah Hale Rosa Jessen, Tim Jessen, Yeong-Seok Jo, Shari Ketcham Kate Leonard-Pasch, Melissa Merrick, Rebecca Minor, Geoff Palmer, Bret Pasch, Erin Posthumus, Nicolas Ramos, Margaret Rheude, and Claire Zugmeyer. I also have my chosen family to thank, for without them I would not have had the strength to continue along the path and whose flamboyant pride never ceases to amaze me. Jean and Bob took me in at age 16, and not only gave me a place to come home to, but a (crazy) family. My sister Briget and nieces Abbigail and Gabrielle have given me a preposterous amount of unconditional love, support and cheerleading. And lastly, to my husband, partner and best friend, Jim, who has gone above and beyond in encouraging and funding my work, explains to people what I do (proudly, succinctly and with a straight face!), makes me laugh until I cry and always brings me joy. 5
TABLE OF CONTENTS
LIST OF TABLES ...... 6
LIST OF FIGURES ...... 8
ABSTRACT ...... 10
INTRODUCTION ...... 12 Literature review ...... 13 Study organism ...... 18 Explanation of dissertation format ...... 20
PRESENT STUDY ...... 21
REFERENCES ...... 24
APPENDIX A. ANNUAL CYCLES IN THE DESERT: BODY MASS, ACTIVITY AND REPRODUCTION IN ROUND-TAILED GROUND SQUIRRELS (XEROSPERMOPHILUS TERETICAUDUS) ...... 29 Abstract ...... 30 Introduction ...... 31 Materials and methods ...... 35 Results ...... 40 Discussion ...... 44 Acknowledgments ...... 52 Literature cited ...... 54
APPENDIX B. SOCIALITY AND GENETIC STRUCTURE IN A POPULATION OF ROUND-TAILED GROUND SQUIRRELS (XEROSPERMOPHILUS TERETICAUDUS): MODEL SPECIES OR OUTLIER? ...... 90 Abstract ...... 91 Introduction ...... 92 Methods ...... 97 Results ...... 103 Discussion ...... 105 Acknowledgments ...... 111 Literature cited ...... 112
APPENDIX C. SOCIALITY, BATEMAN’S GRADIENTS AND THE POLYGYNANDROUS GENETIC MATING SYSTEM OF ROUND-TAILED GROUND SQUIRRELS (XEROSPERMOPHILUS TERETICAUDUS) ...... 135 Abstract ...... 136 Introduction ...... 137 Materials and methods ...... 144 Results ...... 150 Discussion ...... 152 Acknowledgments ...... 159 References ...... 161
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LIST OF TABLES
TABLE A1: Behaviors used in time budget analysis of round-tailed ground squirrels (Xerospermophilus tereticaudus) at the Casa Grande Ruins National Monument, Pinal Co., Arizona (2004-2007)...... 72
TABLE A2: Annual cycles of behavior in round-tailed ground squirrels (Xerospermophilus tereticaudus) at the Casa Grande Ruins National Monument, Pinal Co., Arizona (2004-2007) including litter size (± SE), dates of initial emergence from hibernation of males and females, median estrus based on back calculation from litter emergence, and initial and final observation of initial emergence of litters, and last capture date for males and females ...... 73
TABLE A3: Rankings of the top five models using Akaike’s Information Criterion with a small sample size correction (AICc) in Program MARK to explain the survival (phi) and detection probability (p) of round-tailed ground squirrels (Xerospermophilus tereticaudus) at the Casa Grande Ruins National Monument, Pinal Co., Arizona (2004-2007) ...... 74
TABLE A4: Body mass of male and female round-tailed ground squirrels (Xerospermophilus tereticaudus) at the Casa Grande Ruins National Monument, Pinal Co., Arizona (2004-2007)...... 75
TABLE A5: Proportion of time spent in each behavior category by adult male and female round-tailed ground squirrels (Xerospermophilus tereticaudus) at the Casa Grande Ruins National Monument, Pinal Co., Arizona (2004-2007) ...... 76
TABLE A6. A comparison of the annual body mass and activity periods of sciurids, including the average body mass, dates of emergence for males and females, the length of active period, the increase in mass over the active period, the number of days from female emergence to the start of the mating season, length of mating season, and time spent vigilant and foraging and mean annual precipitation ...... 77
TABLE B1: Rates of agonistic and amicable interactions of round-tailed ground squirrels (Xerospermophilus tereticaudus) at the Casa Grande Ruins National Monument, Pinal Co., Arizona (2004-2007) for male-male, female-female, male- female dyads by adults and juveniles ...... 126
TABLE B2: F statistics (FST, FIT, FIS) from the program FSTAT for female round- tailed ground squirrels (Xerospermophilus tereticaudus) at the Casa Grande Ruins National Monument, Pinal Co., Arizona, per year (2005-2007) and total across all years ± SE ...... 127
TABLE B3: Pairwise FST values of round-tailed ground squirrels (Xerospermophilus tereticaudus) at the Casa Grande Ruins National Monument, Pinal Co., Arizona from the program ARELQUIN for each study plot per year. P- values from jackknifing procedure (10,000) are reported in parenthesis...... 128
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LIST OF TABLES – Continued
TABLE C1: A comparison of reproductive traits of sciurids, including the average percentage of multiple paternity, the marker type used to make that estimate, the average number of mates per female, average litter size at emergence, breeding season length, estrus length, density, and a sociality index...... 176
TABLE C2: Summary statistics from 7 microsatellite loci used for a study of round-tailed ground squirrels (Xerospermophilus tereticaudus) at Casa Grande Ruins National Monument, Pinal Co., Arizona (2004-2007) including species where microsatellite originated; repeated core sequences of thymine, guanine, cytosine, and adenine; allelic richness of microsatellites; range of allele sizes; observed and expected heterozygosity and Hardy-Weinberg equilibrium; Polymorphic Information Content and null allele frequency ...... 179
TABLE C3: Measure of the opportunity for sexual selection of male and female round-tailed ground squirrels (Xerospermophilus tereticaudus) at Casa Grande Ruins National Monument, Pinal Co., Arizona (2004-2007) ...... 180
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LIST OF FIGURES
FIGURE A1: Precipitation (in mm) at the Casa Grande Ruins National Monument, Pinal Co., Arizona (2004-2007). Figure 1a shows the bimodal distribution of precipitation. Figure 1b is photos of the field site from 2005 (a year of high precipitation) and 2007 (a year of drought) ...... 84
FIGURE A2: Parameter estimates of survival probability (Φ) ± SE of round-tailed ground squirrels (Xerospermophilus tereticaudus) at the Casa Grande Ruins National Monument, Pinal Co., Arizona (2004-2007) from the top model in Program MARK based on Akaike’s Information Criterion with a small sample size correction (AICc): Phi(t) p(g) ...... 86
FIGURE A3: Mean litter size (±SE) of 65 litters of round-tailed ground squirrels (Xerospermophilus tereticaudus) at initial emergence above ground at the Casa Grande Ruins National Monument, Pinal Co., Arizona (2004-2007)...... 87
FIGURE A4: Seasonal patterns of body mass of adult male (a) and female (b) round-tailed ground squirrels (Xerospermophilus tereticaudus) at the Casa Grande Ruins National Monument, Pinal Co., Arizona (2004-2007) over emergence, pre- mating, estrus, and pre-hibernation ...... 88
FIGURE A5: Activity budget of adult round-tailed ground squirrels (Xerospermophilus tereticaudus) at the Casa Grande Ruins National Monument, Pinal Co., Arizona (2004-2007) ...... 89
FIGURE B1: Study area for round-tailed ground squirrels (Xerospermophilus tereticaudus) at the Casa Grande Ruins National Monument, Pinal Co., Arizona. The smaller inner squares indicate the locations of two 50-m2 sub-plots and the outer larger squares indicate the 50-m2 buffer areas used for this study during 2005-2007...... 131
FIGURE B2: Regression of pairwise relatedness of participants on rates of agonistic and amicable interactions of adult round-tailed ground squirrels (Xerospermophilus tereticaudus) at the Casa Grande Ruins National Monument, Pinal Co., Arizona (2004-2007)...... 132
FIGURE B3: Estimates of mean relatedness (R) and associated standard error through standard jackknife procedure as calculated by the program RE-RAT for all female round-tailed ground squirrels (Xerospermophilus tereticaudus) in the population at the Casa Grande National Ruins Monument, Pinal Co., Arizona over all four years (2004-2007), all males in the population over all four years, and subpopulation comparison for females in each of the two plots (2005-2007) .... 133
FIGURE B4: Plot of the mean of estimated Ln probability (±SD) by the potential number of populations of round-tailed ground squirrels (Xerospermophilus tereticaudus) at the Casa Grande Ruins National Monument, Pinal Co., Arizona (2005-2007) from the program STRUCTURE, the value of K that maximizes the estimated model averaged log-likelihood, log(P(X|K) indicates the number of clusters ...... 134
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LIST OF FIGURES – Continued
FIGURE C1: Number of mates as determined by genotyped offspring for male and female round-tailed ground squirrels (Xerospermophilus tereticaudus) at Casa Grande Ruins National Monument, Pinal Co., Arizona (2004-2007) ...... 183
FIGURE C2: Overall average relatedness with associated SE between littermates for each litter with >2 juveniles (n=31) for round-tailed ground squirrels (Xerospermophilus tereticaudus) at Casa Grande Ruins National Monument, Pinal Co., Arizona (2004-2007) ...... 184
FIGURE C3: Bateman’s gradient for round-tailed ground squirrels (Xerospermophilus tereticaudus) at Casa Grande Ruins National Monument, Pinal Co., Arizona (2004-2007) ...... 185
FIGURE C4: The relationship between the level of sociality (sociality index, Armitage 1981, Koprowski 1998) and the median average litter size for the sciurid species listed in Table C1 ...... 186
FIGURE C5: The relationship between the level of sociality (sociality index, Armitage 1981, Koprowski 1998) and the average percent of multiple paternity in litters for the sciurid species listed in Table C1 ...... 187 10
ABSTRACT
Social organization of a species may impact behavior, reproductive ecology,
mating system, population genetic structure and overall fitness. A spectrum of sociality
exists from solitary individuals to aggregations to integrated, highly related groups. A
large body of knowledge exists for sociality and life-history characteristics of ground-
dwelling sciurids, including several overarching models to explain the evolution of
sociality. These models predict round-tailed ground squirrels (Xerospermophilus tereticaudus) to be solitary based on small body size (~125g), relatively long period of activity (January-June) and a short period of adult-juvenile overlap. However, previous behavioral observations suggest round-tailed ground squirrels have a clustered matrilineal structure with a suite of social behaviors, suggesting that they may represent a unique outlier in ground squirrel sociality models.
Within the population of round-tailed ground squirrels at the Casa Grande Ruins
National Monument in Coolidge, Arizona, USA, rates of amicable and agonistic interactions between adults were low, with no relationship between relatedness of individuals and rates of social interactions. No population substructure was evident with
Bayesian analyses, global or pairwise FST values, and average relatedness among females
did not differ from males. Contrary to previous behavioral studies, round-tailed ground
squirrels did not have high levels of social behavior, nor did they form significant genetic
subpopulation structuring.
The active season of round-tailed ground squirrels closely followed patterns of
precipitation and peak resource availability. Body mass differed between males and 11
females, across years, and within seasons. Males were heavier than females at emergence,
prior to mating and pre-hibernation, but not when females began gestation. Emergence of litters and litter size are related to amount and timing of winter rainfall. Foraging and vigilance behaviors compose 64-66% of the activity budget, but differ in that males spend
a greater proportion of time foraging, whereas females spend a greater proportion of time
vigilant. Round-tailed ground-squirrels have a polygynandrous mating system. Polygyny
was evident in 2004, 2005, and 2006, and multiple paternity occurred in the majority of
litters with 2.5 sires/litter; litter size was positively correlated with the number of sires.
These findings support predictions generated by sociality models for ground-dwelling
squirrels. 12
INTRODUCTION
Evolution of social organization and behaviors within a group are driven by the
benefits of inclusive fitness, reduced predation risk and increased acquisition of critical
resources that outweigh the costs of increased aggression, parasite and disease
transmission and intraspecific competition, particularly for scarce resources and mating
opportunities (Hamilton 1964, Alexander 1974, Wilson 1975). Social behaviors include
any interaction (e.g., altruistic, amicable, and agonistic) among members of a group of
individuals of the same species that maintains group structure (Slobodchikoff and Shields
1988). There are three levels of hypotheses explaining the origin of group formation and
maintenance of social behaviors: 1) phylogenetic constraint (may not represent an
adaptation to current conditions; Wilson 1975), 2) ecological (non-genetic factors are
necessary and sufficient to explain an observed social system; Alexander 1974), and 3)
genetic (high levels of relatedness among group members are required; Hamilton 1964,
Slobodchikoff and Shields 1988). These hypotheses are not exclusive and likely all have
contributed to the evolution and maintenance of sociality. For example, ecological
conditions may favor group living in to more efficiently exploit a resource, and in time,
groups of individuals that have a higher relatedness could obtain additional benefits
through inclusive fitness (Slobodchikoff and Shields 1988). Ultimately, sociality of a
species affects behaviors, reproductive ecology, mating systems and overall fitness.
Analyses of social behaviors, genetic relationships within groups, and ecological costs and benefits within a phylogenetic framework may lead to insights to the origin of social 13 behaviors, group formation, and maintenance (Slobodchikoff and Shields 1988, Lacey
2000).
Literature review
A continuum of sociality exists from solitary individuals, to aggregates of individuals, to integrated groups of highly related individuals (Lott 1984). Ground- dwelling sciurids exhibit the range of sociality including several species with highly social behaviors (e.g., Olympic marmots, Marmota olympus, Barash 1973; Gunnison’s prairie dogs, Cynomys gunnisoni, Hoogland 1995) and species of isolated solitary individuals (Franklin’s ground squirrels, Poliocitellus franklinii, Iverson and Turner
1972, Murie 1973; woodchucks, M. monax, Maher 2009). Models proposed to describe the levels of sociality in ground squirrels (Armitage 1981; Michener 1983, 1984;
Blumstein and Armitage 1998) are presented below.
The initial model of ground squirrel sociality, the life-history tactic model, was based on a multivariate analysis of life-history characteristics of ground-dwelling sciurids
(Armitage 1981). Sociality was defined as individuals of different ages and sexes sharing space; and the pathway to sociality evolved through retention of daughters within the female’s home range as a way of continuing reproductive investment beyond weaning
(Armitage 1981). This model predicted sociality in ground squirrels evolved in response to predation, the effects of which are evident in the specialized anti-predator behaviors of these animals (e.g., alarm calling; Armitage 1981).
The life-history tactic model (Armitage1981) created five categories of increasing sociality: 1) solitary individuals (e.g., woodchucks); 2) aggregates of individuals (e.g., 14
Belding’s ground squirrels, Urocitellus beldingi); 3) aggregates of females defended by a
male (Arctic ground squirrels, U. parryii); 4) harems where females share burrows and
are associated with a territorial male (Columbian ground squirrels, U. columbianus); and
5) multi-harem colonies (black-tailed prairie dogs, C. ludovicianus). The model also suggested that sociality evolved as a tactic for species with large body size living in environments with growing seasons too short to permit sexual maturity as yearlings.
Large body size provides advantages for reduced predation, increased gut capacity, reduced protein needs, increased fat storage and lower mass-specific metabolism to offset the costs of delayed reproduction (Armitage 1981). However, no relationship between the length of active season with the index of sociality was found; species with the highest indices of sociality included the Olympic marmot with a five-month active season and black-tailed prairie dogs, which do not hibernate. Armitage (1981) suggested that additional research was needed on male mating strategies and female reproductive investment to elucidate the evolution of ground squirrel sociality.
A second classification system of sociality in ground squirrels based classifications on the ability of a male to dominate mating opportunities in a cluster of females and distinguished between litters with extended social associations between juveniles (Michener 1983). The association model (Michener 1983) contained five classifications of sociality: 1) asocial: no territory sharing between males and females, juveniles disperse and establish a territory distinct from either parent, and social interactions are mainly agonistic (e.g., Franklin’s ground squirrels); 2) single-family female kin clusters: a mother and her multi-generational offspring form a moderately 15
cohesive group that is not social with and aggressive towards adjacent groups, males
disperse from the natal area and after the breeding season males and females occupy
distinct home ranges (e.g., Belding’s ground squirrels); 3) female-kin clusters with male
territoriality: adult males maintain their territories beyond the breeding season, defend an
area that overlaps the smaller ranges of several adult females and their offspring,
juveniles from adjacent litters may associate after weaning and mothers show no strong
bias against offspring of adjacent females; dispersal is male biased with males dispersing
farther (e.g., Columbian ground squirrels); 4) polygynous harems with male dominance: the harem male maintains a territory where several females and their offspring live, throughout the active season the male is dominant over all other harem members, juveniles from different litters within a harem frequently and amicably interact after weaning, dispersal is male biased (e.g., Gunnison’s prairie dogs); 5) egalitarian polygynous harems: a male and several females form a cohesive group that maintains and defends a common range, males do not dominate females; litter distinctions are not maintained; dispersal is male biased (e.g., Olympic marmots).
Only slightly different from the life-history model (Armitage 1981), the sociality classification system in the association model (Michener 1983) is loosely based on Emlen
and Oring’s (1977) classification of mating systems and Crook et al.’s (1976)
classification of mammalian social systems in terms of dispersal, mating and rearing
strategies. Only a slight degree of variation in mating systems (degree of polygyny) is
suggested. The association model (Michener 1983) proposes that the driving force behind
the evolution of sociality is increased protection from predation (i.e., group vigilance and 16 alarm calling) and avoidance of inbreeding, with the proximate mechanism of male- biased dispersal forming female based kin clusters; thus eliminating the need for kin recognition.
This association model was updated (Michener 1984) to include the amount of time that adult and juvenile activity patterns coincide, as a solution to the problem of a lack of relationship with active season in the life-history model (Armitage 1981). High social indices were given to ground squirrels where seasonal coincidence of activity was greater than 70% between adult and juvenile ground squirrels (Michener 1984). This suggested that social behaviors evolved as a way to minimize aggressive and competitive interactions due to the timing and sequencing of the annual activity cycle. Michener also suggested that more data on length and synchrony of annual cycles were needed for clarification.
The most recent model, the social complexity model (Blumstein and Armitage
1998) expands upon earlier sociality models and explores the additional benefits and costs of group formation as well as the consequences of social complexity rather than the evolution of complexity itself. The social complexity model continues to suggest that groups are formed to reduce predation risk and/or because of the heterogeneous distribution of critical resources. However, this model also specifies that group size is not an adequate descriptor of the complexity of a social system. In their model a new variable, social complexity, was defined based on the number of possible individuals to interact with (group size) and the types of interactions that are possible among the various roles (e.g., dominant, subordinate, breeder) within the group. This measure of social 17 complexity was regressed against other life-history values and as social complexity increased 1) fewer adult females bred, 2) age of first reproduction increased, 3) litter size decreased, and 4) survival of offspring in the first year increased (Blumstein and
Armitage 1998). Consequently, it is not surprising that the life-history values that were related with social complexity are all means of increasing the number of roles individuals could occupy within the group (i.e., having more non-breeders and juveniles). This model further suggests that kin-selected mechanisms play a role in the evolution of offspring survival and reproductive suppression in ground squirrels (Blumstein and Armitage
1998).
All of these models suggest predation is the main evolutionary factor driving sociality. Resource competition may play a role in the evolution of sociality occurring only under high population densities (Armitage 1981). However, all of these models suggest slightly different proximate mechanisms by which groups are formed (i.e., male biased dispersal, inbreeding avoidance) and differ on how the costs of sociality are mitigated in other life-history characteristics. There are important implications for how groups form in various ground squirrel species based on the associated (indirect) fitness consequences of sociality and the various mating systems. Future studies need to integrate the current proximate mechanisms for sociality, level of genetic relatedness within the group, and fitness consequences of sociality for each group member to find support for assumptions of previous models. Currently, data on social behaviors and genetic relatedness are being collected (Griffin and West 2002; West et al. 2002; Blundell 18
et al. 2004; Matocq and Lacey 2004; Hare and Murie 2007; Gauffre et al. 2009, Túnez et al. 2009, Viblac et al. 2010).
Study organism
Round-tailed ground squirrels (Xerospermophilus tereticaudus) are small (~125 g) ground squirrels that inhabit desert areas of the southwestern United States including southeastern California, southern Nevada, and western Arizona, as well as northeastern
Baja California, and northwestern Sonora, Mexico (Hall 1981). Individuals are typically active from late January to August and otherwise enter an inactive phase or shallow torpor (Dunford 1975). Males emerge first from burrows in late January, mating begins in early March (Ernest and Mares 1987), and young are born in late April to early May with lactation extending through June (Neal 1965). Juvenile dispersal of 29-45% of young occurs during June and July (Dunford 1977a). Models of ground squirrel sociality predict
round-tailed ground squirrels to be solitary or form aggregates in favorable environments
due to small body size, relatively long period of activity, and short period of adult-
juvenile overlap (Armitage 1981). However, previous behavioral observations suggest
round-tailed ground squirrels may be more social with a matrilineal population structure
resulting in clusters of related females (Drabek 1973; Dunford 1977b) suggesting round-
tailed ground squirrels may represent a unique outlier in ground-dwelling sciurid sociality. Patterns of social interactions differed between sexes and among age classes and varied significantly among seasons but were most frequent between suspected kin
(Dunford 1975; Dunford 1977b). In addition, this matriarchal social organization has been used to explain several behaviors (i.e., increased rates of female vocalizations and 19
incidences of burrow sharing; Dunford 1977b). However, little is known about the degree of relatedness within a population, or between participants of social behaviors, thus far no determination of mating system has been made.
Round-tailed ground squirrels are an excellent model species for exploring sociality as their above-ground behaviors are easily observable and previous sociality
models have made several testable predictions about their social behavior, annual cycles,
and mating system (Drabek 1973; Dunford 1975; Dunford 1977a, b). This study will
provide important missing biological data, and serve to test predictions of the models of
ground squirrel sociality on annual cycles, types and rates of behavior, social
organization, levels of genetic relatedness, and mating system of round-tailed ground
squirrels.
Lastly, knowledge of behavior can and should be applied to wildlife
conservation. Variation in social and mating systems may occur in response to
individuals attempting to maximize fitness under local conditions (Bekoff et al. 1984,
Lott 1984, West-Eberhard 1989). Thus, information on behavior, mating and social systems and genetic population structure of round-tailed ground squirrels will have conservation implications for the Palm Springs ground squirrel (X. tereticaudus chlorus),
that is considered threatened by the state of California. Studies of sociality are directly
applicable to conservation of small populations, particularly reproductive ecology and
timing of behavioral activity patterns for effective management plans.
20
Explanation of dissertation format
My dissertation is comprised of three manuscripts. The first manuscript, intended
for submission to Journal of Mammalogy (Appendix A), “Annual cycles in the desert:
body mass, activity and reproduction in round-tailed ground squirrels (Xerospermophilus
tereticaudus)” examines similarity in timing of annual activity cycles, body mass and
reproductive cycles of round-tailed ground squirrels relative to other Arctic and desert ground squirrel species. The second manuscript, intended for submission to Behavioral
Ecology (Appendix B), “Sociality and genetic structure in a population of round-tailed ground squirrels (Xerospermophilus tereticaudus): model species or outlier?” tests predictions of ground squirrel sociality models and examines levels of social behavior in relation to genetic relatedness within the population. The third manuscript (Appendix C),
“Sociality, Bateman’s gradients and the polygynandrous genetic mating system of round- tailed ground squirrels (Xerospermophilus tereticaudus)” is currently in press in
Behavioral Ecology and Sociobiology. In this manuscript, the mating system of round- tailed ground squirrels was defined through genetic analyses and application of
Bateman’s gradients.
I took the lead role in these research endeavors by devising research questions, analytical approaches, selecting the field site, collecting data, creating genetic protocols, processing genetic samples, performing data analyses and interpretations, and writing the manuscripts. Co-authors participated in honing research questions, data interpretation, provided editorial oversight, and logistical and material support.
21
PRESENT STUDY
A large body of knowledge exists for ground-dwelling sciurids in relation to their life-history characteristics and sociality, including several overarching models formulated to explain the evolution of sociality within these taxa (Armitage 1981, Michener 1983,
1984, Blumstein and Armitage 1998). Molecular techniques have recently been applied
(Maher 2006, 2009, 2010; Fairbanks and Dobson 2010) to test these models assesing
both model extremes, solitary individuals and male-dominated polygynous harems. The
unique contribution of this dissertation includes a combination of classic field techniques
and current molecular techniques to examine levels of social behavior, genetic
relatedness within the population, mating system, timing of annual cycles and behavior of round-tailed ground squirrels, a potential model outlier. Methods, results and conclusions
of this study are presented in the papers appended to this dissertation. The following is a
summary of the most important findings.
Round-tailed ground squirrels in the Sonoran Desert have similar annual activity
patterns to Arctic ground squirrels. However, the timing of the active season is earlier in
the year most likely due to patterns of precipitation and peak resource availability.
Annual patterns of body mass at emergence are similar to patterns for other ground
squirrels but with differences between males and females, across years, and time
intervals. Males were heavier than females at emergence, prior to mating and to
hibernation, but not during the mating period when females began gestation. Emergence
of litters and litter size were related with amount and timing of winter rainfall. Foraging
and vigilance behaviors composed the majority of the activity budget of round-tailed 22
ground squirrels, but t males spend a greater proportion of time foraging, whereas
females spend a greater proportion of time vigilant.
In previous behavioral studies, round-tailed ground squirrels had a matrilineal social structure (Dunford 1977b). However, round-tailed ground squirrels were predicted to be solitary by all models of ground squirrel sociality. I assessed levels of social behaviors combined with microsatellite genotyping to investigate social and genetic structure of the population. Rates of amicable and agonistic interactions between adults were low (≤0.69 interactions/hour) with no relationship between relatedness of individuals and rates of either amicable or agonistic interactions. No population sub- structure was evident with Bayesian analyses, global or pairwise FST values, and average
relatedness among females were not significantly different than males. Contrary to
previous behavioral studies, our population of round-tailed ground squirrels does not
have high levels of social behavior, nor exhibit subpopulation genetic structure.
Through current genetic techniques, I classified round-tailed ground-squirrels to
have a polygynandrous mating system, which fits predictions generated from ground
squirrel sociality models. Polygyny was evident in all years studied except 2007, when
population size was reduced compared to other years. Multiple paternity occurred in the
majority of litters (55%) with 2.52 ± 0.26 sires/litter ± SE; litter size was positively
related with the number of sires. Through indirect analysis of paternity, I found 21 litters
(68%) with an average relatedness of 0.5 or less. Males had a greater opportunity for
sexual selection (Is=1.60) than females (Is=0.40); the Bateman’s gradient, which assesses
the intensity of sexual selection, was also greater in males (1.07 ± 0.04SE) than females 23
(0.82 ± 0.08SE). When evaluating predictions of sociality models among sciurid species,
I found a negative relationship between the level of sociality with litter size and the average percentage of multiple paternity within a litter. Thus, genetic information and reclassification of mating systems presented in the following appendices support the general predictions of the sociality models for the ground-dwelling squirrels.
24
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29
APPENDIX A.
ANNUAL CYCLES IN THE DESERT: BODY MASS, ACTIVITY AND
REPRODUCTION IN ROUND-TAILED GROUND SQUIRRELS
(XEROSPERMOPHILUS TERETICAUDUS)
Munroe, K. E. and J. L. Koprowski
(In the format of the Journal of Mammalogy)
30
Karen E. Munroe School of Natural Resources and the Environment The University of Arizona Tucson, Arizona 85721 Phone: (520) 490-8948 email: [email protected]
Desert ground squirrel annual cycles
Annual cycles in the desert: body mass, activity and reproduction in round-tailed ground squirrels (Xerospermophilus tereticaudus)
KAREN E. MUNROE* AND JOHN L. KOPROWSKI
Wildlife Conservation and Management, School of Natural Resources and the
Environment, 325 Biological Sciences East, The University of Arizona, Tucson, AZ 85721
520-490-8948
Target journal: Journal of Mammalogy
ABSTRACT
Terrestrial species in harsh environments must match their annual activity periods to the temporal availability of resources and favorable climate ranges. We predicted that ground squirrels in desert environments would have similar annual activity periods, annual cycles of body mass and daily activity patterns to ground squirrels in arctic environments. We
demonstrate that round-tailed ground squirrels (Xerospermophilus tereticaudus) in the
Sonoran Desert have similar annual activity patterns to arctic ground squirrels. However,
timing of the active season in the desert was shifted earlier most likely due to patterns of
precipitation and peak resource availability. Analyses of annual cycles of body mass 31
revealed patterns similar to other ground squirrels at emergence, but differed between
males and females, across years, and seasons. Males were heavier than females at
emergence, prior to mating and pre-hibernation, but not during mating season when
females began gestation. Emergence of litters and litter size were related with amount and
timing of winter rainfall, but not female body mass or timing of litter emergence.
Foraging and vigilance behaviors compose the majority of the round-tailed ground squirrel’s activity budget, but differ in that males spend a greater proportion of time foraging, whereas females spend a greater proportion of time vigilant. Survival estimates varied greatly and ranged from <0.01 to 1.00 with the lowest survival during the winter months. Harsh climates and interannual variation in precipitation contribute significantly to annual variation in mean body mass, timing of activity and reproduction, and litter size and provides strong evidence for the important role that environmental variation plays in ground squirrel ecology.
KEY WORDS
Arizona, estrus, life-history variation, litter size, precipitation, Sciuridae, Sonoran Desert,
*Correspondent: [email protected]
INTRODUCTION
The amount of time and energy that an animal allocates to a specific behavior is
affected by a variety of physiological, morphological and environmental factors
(Belovsky and Slade 1986; Lockard 1978). These factors may interact and result in trade- 32
offs among activities which can differ between various sex and age classes within a population (Moen 1973). For example, sex-specific behaviors (e.g., lactation, mating displays) or sexual dimorphism may affect energy allocation to other behaviors, thus influencing time allocation to various behaviors. Observed time and energy allocation within a species have underlying evolutionary implications (Orians 1961), particularly for animals in harsh environments.
The harsh environments of the arctic and desert share, extreme temperatures and minimal, but temporally variable precipitation that typically creates a pulse of peak resource availability (Went 1948). Arctic environments are characterized by extreme low winter temperatures with precipitation mostly in the form of snow. Once snow begins to melt and water becomes available, arctic plants exit dormancy and begin rapid growth
(Billings and Mooney 1968). Desert environments are characterized by extremely low amounts of precipitation, less than 250 mm per year. In the desert, the life-history of annual plant species is closely coupled to periods of winter rain (Venable 2007). Some annual plant seeds remain dormant and delay germination and some plants postpone reproduction until favorable conditions occur, such as a pulse of precipitation, creating a surge of plant productivity when conditions are optimal (Cohen 1966; Noy-Meir 1973;
Venable 2007). In the Chihuahuan and Mohave deserts, mass germination and rapid seedling growth are triggered by the pulse of winter rains (Beatley 1974; Kemp 1983).
Animal species living in harsh environments possess an array of physiological and behavioral adaptations to take advantage of peak resource availability, including annual 33
shifts in timing of behavioral activity, annual cycles of body mass, timing of mating and
daily activity patterns (Bullard 1972; Ward 2009).
Knowledge of ground-dwelling sciurids of the genera Cynomys, Ictidomys,
Marmota, Otospermophilus, Spermophilus, and Urocitellus is mostly based on studies of
temperate or arctic populations (Michener 1984). In these environments, ground squirrels
have highly seasonal cycles defined by winter hibernation and a spring-summer active
season when mating, gestation, lactation, emergence and growth of juveniles, and pre-
hibernation mass gain occurs (Michener 1984). Timing and duration of the active season
is shaped by availability of resources typically associated with climate and elevation
(Bronson 1979; Dobson and Davis 1986; Dobson et al.1992; Michener 1979; Morton and
Sherman 1978; Murie and Harris 1982), with short active seasons for squirrels in harsh
environments at high elevations and northern latitudes compared to species in temperate
environments (Armitage 1981; Barash 1974; Bronson 1979; Michener 1979, 1984;
Morton and Sherman 1978; Murie and Harris 1982). Emergence from hibernation in
harsh environments is related with onset of plant productivity (Michener 1984). In
addition, the length of the active season to maximize body mass gain for lactation and
hibernation in adults and growth in juveniles is compressed (Balph 1984; Kenagy et
al.1989; Michener 1979).
The degree of sociality has been hypothesized to increase with environmental
harshness (higher altitudes and latitudes) where shorter growing seasons lead to delayed
juvenile dispersal, prolonged protection and provisioning by parents, and increased social
organization and behaviors (Armitage 1999, 2007; Barash 1974; Ebensperger 2001; Hare 34
and Murie 2007). Knowledge of how species apportion their time and the environmental
factors that contribute to such allocations is important to understand strategies of survival and reproductive success as well as the evolution of social behaviors in ground-dwelling sciurids. Analysis of time-activity budgets may elucidate how animals allocate time and
energy within the constraints of their physiology and environment (e.g., habitat,
conspecifics, predators and seasonality).
As a group, desert ground squirrels deviate from the single annual pattern of activity periods and cycles of body mass. For example, Harris's antelope squirrels
(Ammospermophilus harrisii) do not hibernate and are active throughout the year (Neal
1965a; Neal and Wood 1965), Mexican ground squirrels (I. mexicanus) are active March
through September (Schwanz 2006), Mohave ground squirrels (Xerospermophilus
mohavensis) are active February through July (Bartholomew and Hudson 1960), and rock
squirrels (O. variegatus) vary greatly in their hibernation patterns and are active from 6-
11 months per year in various parts of their range (Oaks et al. 1987).
Little is known about round-tailed ground squirrels (X. tereticaudus) and their
annual activity patterns, variation in annual cycles of body mass, daily activity trade-offs,
and reproductive patterns in relation to desert environmental conditions (Ernest and
Mares 1987). We predict that round-tailed ground squirrel seasonal variation in mass and
annual reproductive patterns follow peak resource availability to minimize the impact of
energetically costly activities (i.e., gestation, lactation, and pre-hibernation weight gain) similar to arctic and temperate ground squirrel species. Furthermore, round-tailed ground squirrels should modify their daily activity patterns to minimize energy expenditures 35
while maximizing survival and reproductive success. The purpose of this study is to
describe annual variation in timing of activity, reproductive patterns, and litter size, and
seasonal changes in daily activity patterns, and body mass and in round-tailed ground
squirrels in relation to variation in timing and amount of annual precipitation.
MATERIALS AND METHODS
Study organism – Round-tailed ground squirrels inhabit desert areas of the southwestern United States including southeastern California, southern Nevada, and western Arizona, as well as northeastern Baja California, and northwestern Sonora,
Mexico (Hall 1981). What little is known about annual cycles of round-tailed ground squirrels is primarily anecdotal. Round-tailed ground squirrels may be active from late
January to August and enter an inactive phase or shallow torpor (Dunford 1975). Round- tailed ground squirrels emerge from hibernation earlier than most other ground-dwelling sciurids (with the exception of M. monax: Davis 1977; reviewed in Michener 1984).
Males emerge first from burrows in late January, mating begins in early March (Ernest and Mares 1987), young are born in May and lactation extends through June (Neal
1965a). A second litter may be produced (Neal 1965b; Reynolds and Turkowski 1972).
The vast majority (75-80%) of the variation in litter size was accounted for by variability in rainfall between October and February; each 25 mm of rain during this period increased mean litter size by 1 (Reynolds and Turkowski 1972). Sociality may be environmentally (Munroe and Koprowski in review) rather than kin driven (Dunford
1977). 36
Study site – We monitored a population of round-tailed ground squirrels at Casa
Grande Ruins National Monument in Coolidge, Pinal County, Arizona, from January
2004 to June 2007. The park is dominated by relatively evenly dispersed creosote bushes
(Larrea tridentata) with occasional barrel (Opuntia sp.), saguaro (Cereus giganteus) and
planted ornamental cacti and trees around the visitor center and picnic area. The 259-ha park is surrounded on two sides by agricultural fields, and a retail shopping center and a residential area.
The climate of the Sonoran Desert is characterized by extreme summer temperatures and bimodal precipitation patterns that include a winter-spring season where most of the precipitation occurs and a summer season with intense monsoonal thunderstorms and associated flash floods (Phillips and Comus 2000; Turner and Brown
1994). Average annual precipitation for Coolidge, Arizona is 244.1 mm with 61% falling during winter (October-March) and 33% during monsoons (July-September; National
Climatic Data Center, Casa Grande National Ruins Monument Station; long term averages based on data from 1971 to 2000, Fig. 1a). In 2005-2006, Coolidge experienced a drought receiving only 51% of the normal winter precipitation with no precipitation
from 18 October through 11 March (Fig. 1). Average daily minimum and maximum
temperatures were 1oC to 20oC in January and 23oC to 42oC in August. Daytime
temperatures regularly exceed 46oC in May, through August (National Climatic Data
Center, Casa Grande National Ruins Monument Station).
37
Trapping and handling – In 2004, we began live trapping round-tailed ground
squirrels within the perimeter of the Monument. In 2005, we established two 50-m2 study
plots with an outer 50-m2 buffer area at two random locations. We used Sherman live traps (H.B. Sherman Traps, Inc, Tallahassee, Florida) baited with sunflower seeds and/or peanut butter to trap adult squirrels at active burrows during the day. We checked traps at intervals of 2 h or less depending on ambient temperature. We used a cloth handling cone to immobilize squirrels (Koprowski 2002) for processing and released all individuals at the point of capture. We measured body mass (± 5 g) with a Pesola spring scale (Baar,
Switzerland). We determined sex and reproductive condition upon initial capture. To
determine reproductive condition we visually inspected the testis position (abdominal,
inguinal, or scrotal) for males. For females we visually inspected teats to assess degree of distension, alopecia, and pigmentation (Larsen and Taber 1980) and inspected the vulva
to determine swelling indicative of estrus. We marked individuals with a unique
freezemark, applying spray liquid nitrogen for just under 2 sec (Koprowski 1996; Rood
and Nellis 1980) and hair dye (Clairol Balsam Lasting Color, True Black #618, Procter &
Gamble, Cincinnati, Ohio) for permanent and immediate identification in the field. We
counted litter size at the first appearance of juveniles above ground. We also
systematically searched the Monument, monthly for marked squirrels that dispersed to
examine dispersal and turnover rate. All procedures followed guidelines of the American
Society of Mammalogists for animal care and use (Sikes et al. 2011). Trapping and
handling were approved by The University of Arizona Institutional Animal Care and Use 38
Committee (IACUC number 07-026, 04-009), the Arizona Game and Fish Department, and the National Park Service.
Data collection and analysis – We began visiting field sites in early January to assess squirrel activity through active burrows and to pre-bait. We trapped round-tailed
ground squirrels an average of four days a week from January through August 2004 and
2005, and January through May 2006 and 2007. Litter size and emergence date of litters
were recorded at first sighting above ground. Parturition and estrous dates for each adult
female who successfully reared a litter were back-calculated from the date of litter
emergence. Time between litter emergence and estrus was estimated at 56 days, based on
the median of previous estimates for gestation and ontogeny of young X. tereticaudus
(Neal 1965b, 1965c; Reynolds and Turkowski 1972). Median gestation time was
estimated at 30 days, based on the gestation of captive round-tailed ground squirrels
(Neal 1965b; Reynolds and Turkowski 1972), which enabled us to calculate date of estrus
for each mother. We defined length of the mating season for the population as the number
of days between the dates of the back calculated first and last estrus. We separated
seasonal activity into four time intervals: 1) emergence (two weeks after initial
observation of above ground activity), 2) pre-mating (the period between the end of the
two weeks after emergence but before estrus), 3) mating/gestation season (dates of back- calculated estrus from litter emergence), and 4) pre-hibernation (post-weaning). We used linear regression to assess effects of female body mass at emergence, the timing of litter emergence, and the amount of precipitation on litter size. To assess annual changes in 39
body mass, we assessed mean body mass at 4 intervals of activity each year for males and
females. We compared body mass with time intervals, year, and sex via a Poisson regression with a log link function, two-way analysis of variance (ANOVA), one-way analysis of variance and Tukey-HSD post-hoc analyses.
Behavioral observations and analysis – We used binoculars to observe adult round-tailed ground squirrels during periods of daily activity from a distance of approximately 40 m. We obtained scan samples every 10 min to document which individuals were present and 9-min focal animal observation to determine individual behavior and interaction rates (Altmann 1974). We categorized behaviors as social behaviors/physical contact (amicable or agonistic), digging, collecting nest matter (i.e., dried grasses), foot drumming (i.e., response to a predator or human), traveling, basking, foraging, and vigilant (i.e., an upright posture; Table 1). Because animals did not always
remain in view for the entire nine min focal animal observation, we converted
interactions to rates when appropriate. We applied arcsine root transformation to all
proportion data to satisfy normality assumptions (Zar 1999). We used a logistic
regression with a identity link function to assess differences among proportion of
behaviors across years between sexes and a two-way ANOVA to assess differences in behaviors.
We used Program MARK (warnercnr.colostate.edu/~gwhite/ mark/mark.htm;
White and Burnham 1999) to investigate the overall survival and detection rate of individual within our study areas. We constructed monthly encounter histories from 40
behavioral observations for individually marked squirrels. We used an information-
theoretic approach and selected the best-approximating models using Akaike’s
Information Criterion (AICc; Burnham and Anderson 2002). We started with basic
models using an identity design matrix and then modified the design matrix to represent
the difference in time periods and monthly effort. We used JMP-IN (SAS Institute Inc.
2003) to perform all analyses. All means are reported ± SE.
RESULTS
We captured 351 unique round-tailed ground squirrels (98 adult females, 114 adult males, 51 juvenile females, 88 juvenile males) from February 2004 to May 2007.
Of the 40 adult females on our study plots over the 3 years (2005: n=18; 2006: n=12;
2007: n=10), only two were present in consecutive years; one female stayed on a plot
during the study (2006) and one female immigrated to a plot, did not disperse after
breeding, and did not produce a litter in the subsequent year. We did not detect dispersal
between plots.
Annual timing of activity – Winter emergence was asynchronous between the
sexes (Table 2). Males emerged in late January to early February and females emerged
from early to late February. In three of four years, except 2005, a short interval (~ 2
weeks) occurred between female emergence and the start of estrus (pre-mating interval).
Initial emergence of litters was observed from late April in 2004 and 2005 but was
delayed to mid-to-late May in 2006 and 2007. In each year, litters emerged during a 41
single, short period indicating a single pulse of estrus. Average length of the mating
season over all four years (12.25 ± 1.1 days, Table 2) was back calculated from the
timing of litter emergence.
Adult males and females disappeared through the year, with the majority of
disappearances presumed to reflect immergence into hibernation (Table 2). In 2004, the
last male trapped was in early June, whereas the last female trapped was in late July. In
2005 the last female and male captured were in late August. In 2007 the last male was captured before litters emerged (Table 2). Within our study area, both males and females experienced >95% turnover in all 4 years, based on the number of individuals captured in the emergence and pre-mating period that were previously marked. We searched systematically at least monthly in adjacent areas for marked individuals and found none.
The top model of our five candidate models was a time dependent survival and a sex specific detection probability (Phi(t) p(g); Table 3). Our detection probability for
females was 0.69 ± 0.05 and males 0.35 ± 0.08 with survival estimates ranging from
<0.01 to 1.00 with the lowest survival during the winter months (Fig. 2).
Reproduction –The percentage of females that reproduced varied among years.
From 2005-2007 the percent of females producing a litter declined from 100% to 50% to
20%. For 65 litters, the date of initial emergence of juveniles from the natal burrow is
known with an overall mean litter size of 4.1 ± 0.38 young/litter (range: 1-13 young/litter,
Fig. 3). Emergence date did not explain variation in litter size (linear regression, F = 0.27,
d.f. = 1,64, P = 0.60). The average litter size differed between years (ANOVA: F = 4.3, 42
d.f. = 3,61, P = 0.008), with 2005 having the largest average litter size (6.15 ± 0.41
young/litter) and 2007 having the smallest average litter size (3.22 ± 0.72 young/litter).
Litter size and average annual precipitation were positively related (y = 0.011x + 3.6986,
R2 = 0.10, F = 7.3, d.f. = 1, 64, P = 0.009). Female body mass at emergence did not
explain litter size (linear regression, F = 0.09, d.f. = 1, 28, P = 0.77). The onset and length
of the mating season varied in all 4 years (Table 2). The timing of litter emergence was
unimodal and no female produced (n = 40) two litters in a single year. During the time of
estimated estrus, all males were scrotal in all years (n = 58).
Change in body mass – Body mass differed among years (χ2 = 134.1, P < 0.0001); with an interaction between sexes and among seasons (χ2 = 38.2, P < 0.0001), and
between sexes among years (χ2 = 9.3, P = 0.0258; Table 4, Fig. 4). Over all years, males
were heavier (149.0 ± 2.8 g) than females (139.0 ± 2.7 g; t = -2.6, d.f. = 233, P = 0.009).
Males were heavier than females at emergence, pre-mating, and pre-hibernation (two-
way ANOVA, F = 15.5, d.f. = 7, 227, P < 0.0001); but not during mating period when
females were beginning gestation. Males differed in weight at emergence among years
(ANOVA, F = 3.23, d.f. = 3, 59, P = 0.03, Fig. 4a). Females differed in weight at
emergence and pre-hibernation among years (ANOVA: emergence: F = 7.31, d.f. = 3, 28,
P = 0.001; pre-hibernation: F = 4.01, d.f. = 3, 16 P = 0.04, Fig. 4b). Male body mass
differed among intervals (ANOVA: F = 13.2, d.f. = 3, 114, P < 0.0001; Fig. 4a). Males
increased to their heaviest mass before hibernation. Females similarly increased in body 43
mass during mating and pre-hibernation (ANOVA, F = 20.8, d.f. = 3, 116, P < 0.0001;
Fig. 4b).
Behavior – Eighty-one round-tailed ground squirrels (2007: five males, seven females; 2006: 11 males, 12 females; 2005: seven males, 17 females; 2004: seven males,
15 females) were observed for 8,278 min. We had 880 observation periods for males and
472 observation periods for females, however, females were observed above-ground for a
greater length of time (1.9: 1min female: male; t = 5.53, d.f. = 80, P < 0.0001). The
proportion of behaviors did not differ among years (χ2 = 0.05, P = 0.83) so years were
combined for further analyses. Males and females differed in the proportions of the time
spent in the various behaviors (two-way ANOVA, F = 3.0, d.f. = 7, 358, P = 0.004, Table
5, Fig. 5). In females, the majority of time was devoted to vigilance (33%), feeding (31%)
and basking (20%); in males, the majority of time was devoted to feeding (41%),
vigilance (25%) and basking (21%); sexes differed in vigilance (Tukey-Kramer HSD
multiple comparisons, difference in mean 0.93 ± 0.15) and foraging (Tukey-Kramer HSD
multiple comparisons, difference in mean -0.50 ± 0.15). We predicted that during
gestation and lactation females would spend a greater proportion of time foraging than
males and, after litter emergence, females would spend a greater proportion of time being
vigilant than males (Gittleman and Thompson 1988; Kurta et al. 1989; Stebbins 1977).
Females foraged a greater proportion of time than males between estrus and litter
emergence (t = 2.54, d.f. = 180, P = 0.01), but were not vigilant a greater proportion of
time than males (t = 1.30, d.f. = 128, P = 0.19). After litter emergence, females were more 44 vigilant than males (t = 1.90, d.f. = 50, P = 0.06), but females did not forage a greater proportion of time than males (t = 0.85, d.f. = 37, P = 0.40).
DISCUSSION
The annual activity cycle of ground squirrels consists of an inactive season and an active season characterized by emergence from hibernation, mating, gestation, lactation, emergence and growth of juveniles, and immergence into hibernation (Michener 1983,
1984). Adult males usually emerge from hibernation before females, and mating occurs shortly after emergence of adult females (Barnes 1996). The general patterns observed in annual activity, annual cycles of body mass, daily activity of males and females, and reproductive patterns of round-tailed ground squirrels are similar to ground squirrels in northern latitudes (e.g., Columbian ground squirrels, U. columbianus; European ground squirrel, Spermophilus citellus; Franklin’s ground squirrels, Poliocitellus franklinii;
Richardson’s ground squirrels, U. richardsonii; Table 6). Furthermore, the interannual variance in body mass, timing of reproduction, litter size, and activity budget results provides additional evidence for the importance of environmental variation in the evolution of ground squirrel ecology.
Annual timing of activity – A major difference in the annual activity patterns of round-tailed ground squirrels is the early onset of the active season in round-tailed ground squirrels (Table 4). Environmental factors may synchronize individuals with each other and with their environment (Heller and Poulson 1970). For hibernating ground 45 squirrels, timing of emergence is related to climatic variables such as snow cover
(Bronson 1979, Phillips 1984), snow depth (Morton and Sherman 1978, Murie and Harris
1982), air temperature (Knopf and Balph 1977, Murie and Harris 1982) and soil temperature (Iverson and Turner 1972, Michener 1978, Wade 1950); in desert ground squirrels, timing of emergence is likely also related to similar climatic variables and therefore is triggered to match patterns of precipitation and peak resource availability in the Sonoran Desert (Bullard 1972; Ward 2009). Litters emerge during late spring when high resource requirements by adult females for lactation and hibernation fattening and by juveniles for growth correspond with high plant productivity. The long active season is likely due to the mild winters and patterns of precipitation. The asynchrony of emergence and immergence of round-tailed ground squirrels was similar to other ground squirrel species, with males emerging and immerging earlier than females (e.g., Belding’s ground squirrels: Morton and Sherman 1978; Richardson’s ground squirrels, U. richardsonii: Clark 1970, Yeaton 1972, Michener 1977; Unita ground squirrel, U. armatus: Slade and Balph 1974, Knopf and Balph 1977; Golden-mantled ground squirrel,
S. lateralis: Mullally 1953, Skryja and Clark 1970, Bronson 1977; long-tailed ground squirrel U. undulates: Mitchell 1959, Franklin’s ground squirrel, Poliocitellus franklinii:
Sowls 1948, Iverson and Turner 1972; Columbian ground squirrels: Shaw 1925a,
Manville 1959; white-tailed prairie dog, Cynomys leucurus: Stockard 1929, Bakko and
Brown 1967, Clark 1973, reviewed in Michener 1984, Table 6). The annual chronology of hibernation of arctic, subarctic and temperate species is remarkably similar (arctic ground squirrel: Hock 1960, McLean and Towns 1981, Buck and Barnes 1999; 46
Columbian ground squirrel: Murie and Harris 1982, Young 1990; and the golden-mantled
ground squirrel, Callospermophilus lateralis: Bronson 1979, Phillips 1984); where
individuals emerge from and immerge into hibernation during the same 2-3 weeks within
each calendar year. Richardson’s ground squirrels in Alberta, Canada, are an exception
to this pattern emerging and immerging ≥1 month earlier than other species (Michener
1992).
The timing and length of activity in Mexican ground squirrels in the Chihuahuan
Desert is more similar to northern ground squirrel species than round-tailed ground squirrels (Schwanz 2006). This reflects differences in precipitation and temperature patterns between the Chihuahuan and Sonoran deserts. The Chihuahuan Desert receives a
greater proportion of annual precipitation in summer, than in winter and experiences
cooler summer and winter temperatures than the Sonoran Desert (Reynolds et al. 2004).
The overall length of annual activity period in round-tailed ground squirrels is short
compared to Mexican and Mohave ground-squirrels (Bartholomew and Hudson 1960;
Schwanz 2006), but similar to arctic ground squirrels (Buck and Barnes 1999), Anatolian
ground squirrels, (S. xanthoprymnus; Gür and Gür 2005), Cascade golden-mantled
ground squirrel (Blake 1972; Jameson 1964), European ground squirrels (Millesi et al.
1999a) and thirteen-lined ground squirrels (McCarley; Table 6).
Reproduction – It has been suggested that timing of reproduction is especially
important at high altitude or other regions with short and sharply defined growing
seasons (Morton and Sherman 1978); therefore we expected round-tailed ground squirrels 47
should time reproduction with periods of peak resource availability, rather than follow
the general pattern in timing of reproduction of ground squirrels. In most ground
squirrels species, females enter estrus within a few days of emergence from hibernation
(reviewed by Gür and Gür 2005). However, round-tailed ground squirrels emerged in late
January to early February and entered estrus approximately 4 weeks later except in 2005, after an early period of high rainfall (Fig. 1). Postponed estrus also occurs in Mexican ground squirrels (Schwanz 2006) and thirteen-lined ground squirrels (I. tridecemlineatus) in Texas (McCarley 1966). Estimated mating season length for round-tailed ground squirrels (12.25 ± 3.75 days) is shorter than most ground squirrels, although comparable season lengths occur in thirteen-lined ground squirrels (Hohn 1966), Idaho ground squirrels (Spermophilus brunneus: Sherman 1989), Belding’s ground squirrels (Morton and Sherman 1978; Sherman 1977), and arctic ground squirrels (U. parryii: Carl 1971;
Hubbs and Boonstra 1997; Lacey et al. 1997; Table 6). The short length of the mating season suggests significant competition for females, given the polygynandrous mating system and sperm competition (Munroe and Koprowski 2011). Furthermore, round-tailed ground squirrels do not have two litters or the ability to enter estrus if they fail to produce an initial litter (Cockrum 1982; Jaeger 1961; Neal 1965b; Reynolds and Turkowski
1972), but rather postpone estrus. We found support for the earlier finding that mean litter size increased with precipitation (Reynolds and Turkowski 1972).
Patterns of body mass – Changes in body mass over the active season occur in ground squirrels (e.g., Boag and Murie 1981; Buck and Barnes 1999; Fagerstone 1988; 48
Gür and Gür 2005; Knopf and Balph 1977; Michener and Locklear 1990a; Morton 1975;
Schwanz 2006). In many species of ground squirrels, males emerge from hibernation at a
relatively low mass and continue to decrease to their lowest body mass at the end of
mating season and increase before hibernation (Anatolian ground squirrels, Gür and Gür
2005; Arctic ground squirrels, Buck and Barnes 1999; McLeand and Towns (1981);
European ground squirrel, Millesi et al. 1999; Richardson’s ground squirrel, Michener
and Locklear 1990a; Mexican ground squirrels, Schwanz 2006; Unita ground squirrel,
Knopf and Balph 1977; Wyoming Ground Squirrels, U. elegans; Buck and Barnes 1999;
Fagerstone 1988). Round-tailed ground squirrels generally followed this pattern. Males emerge from hibernation at their lightest mass of the year with abdominal testes and increase in body mass throughout the active period. Body mass of females increased during pre-mating, mating and pre-hibernation in most years. In arctic and European ground squirrels, males emerge at a greater body mass than females, however, quickly lose mass through the mating season until equivalent to females and then increase to their heaviest weight just prior to hibernation (Buck and Barnes 1999; Millesi et al. 1999a).
Due to the asynchrony of reproductive events in females, the change in body mass during
gestation and lactation (i.e., parturition) may be largely masked in population averages.
Behavior – Time spent foraging is generally considered critical in meeting the energy demands of maintenance, growth, and reproduction (Altmann 1974), and for ground squirrels, building energy reserves for hibernation (Armitage 1981; Armitage et
al. 1996). Time allocated to other behaviors (e.g., vigilance and basking) reduces time 49 available for foraging, however, may lead to increased survival and reproductive success
(Armitage et al. 1996; Ferron et al. 1986). Vigilance and foraging comprise the largest proportion of round-tailed ground squirrels time budgets, with females trading off forging opportunities for increased rates of vigilance. Columbian ground squirrels (Betts 1976),
Olympic marmots (M. olympus; Barash 1973), spotted ground squirrels (X. spilosoma;
Streubel 1975), thirteen-lined ground squirrels (Streubel 1975), Wyoming ground squirrels (Zegers 1981), and yellow-bellied marmots (M. flaviventris; Armitage et al.
1996) show similar proportions of time foraging. The influence of this behavioral trade- off is reflected in the overall difference in body mass between males and females.
Seasonal changes in food availability and energy requirements may affect feeding time for round-tailed ground squirrels as documented for a variety of other mammals (Barash
1980; Kenagy et al.1989; Wauters 2000). Round-tailed ground squirrels ingested not only annual forbs and grasses produced after winter rains, but in periods of drought, they ingested all parts of the creosote bush (i.e., flowers, inner cambium, leaves, and seeds;
Munroe and Koprowski, unpubl. data). The proportion of time spent vigilant is equal to or less than most species of ground squirrels, except for Cascade golden-mantled ground squirrel (Kenagy et al. 1989), Columbian ground squirrels (Betts 1976), and yellow- bellied marmots (Armitage et al. 1996). Compared to tree squirrels, round-tailed ground squirrels spent a greater proportion of time vigilant and basking and foraged less
(Koprowski and Corse 2005; Wauters et al. 1992). This reduced time foraging may be due to higher quality of forage and need to reduce thermal stress. 50
Female round-tailed ground squirrels spent a greater proportion of time foraging and vigilant than males during the interval between estrus and litter emergence. Yellow- bellied marmots and Alpine marmots exhibit similar differences between sexes in the proportion of foraging and vigilance (Armitage et al. 1996; Sala et al. 1992) during reproductive effort. Female California ground squirrels foraged more than males, but were not more vigilant during reproductive stages (Owings et al. 1979). In North
American red squirrels (Tamiascurus hudsonicus), the proportion of time of various behaviors did not differ between the sexes during the mating season (Ferron et al. 1996); but female Mt Graham red squirrels (T. h. grahamensis) spent more time foraging and
vigilant than males during the breeding season (Greer and Koprowski 2009). This
difference in behavior may be due to avoidance of daily environmental extremes,
particularly in this subspecies located at the southern terminus of the red squirrel range.
The Sonoran Desert, like many arctic ecosystems, is characterized by a suite of
harsh environmental conditions (Phillips and Comus 2000; Turner and Brown 1994).
Adaptations for coping with such harsh conditions include timing annual activity periods
to coincide with peak resource availability and rapid reproduction and rearing of young, followed by long periods of reduced activity (i.e., hibernation or estivation). It is not surprising, given similar resource constraints that round-tailed ground squirrels exhibit similar annual cycles of body mass and activity periods to that of Arctic squirrels shifted earlier to take advantage of the pulse of peak resource availability (Bullard 1972; Ward
2009). Seasonal changes in rodent densities are more similar in tundra and the desert than 51 in temperate areas; probably due to a similar pulse in resource availability (Jedrzejewski and Jedrzejewski 1996).
High temperatures, diversity of predators, and extreme variability in rainfall events and amounts present additional challenges for desert-dwelling ground squirrels.
Population turnover for round-tailed ground squirrels was incredibly high in our population and not similar to previous studies of round-tailed ground squirrels (Drabek
1973; Dunford 1975) or other ground squirrel species (Boag and Murie 1981; McCarley
1966; Michener and Locklear 1990b; Morton and Sherman 1978), with the exception of male Richardson’s ground squirrels (over 80% turnover; Michener and Locklear 1990a).
In previous studies, over-winter losses of round-tailed ground squirrels were low with only 0-43% loss for females and 16-62% loss for males (Drabek 1973; Dunford 1975).
However, these animals were not permanently marked, but classified as a continuing cohort based on their adult weight at emergence; therefore it is possible that this turnover rate includes adult immigrants, but we could not distinguish death and dispersal, but low survivorship and high turnover may be somewhat common in desert ground squirrel populations, especially following severe droughts. Our findings suggest relatively low survival rates particularly during the winter months.
Analyses of behavior are important for understanding how animals contend with energy demands, particularly in harsh and variable environments (Orians 1961), and how time and energy allocation affect individual survival and reproductive success.
Differences in timing of activity patterns and allocation of time to behaviors may suggest different constraints on males and females, thus impacting reproductive ecology, and 52
potentially the degree of sociality in ground-dwelling sciurids (Armitage 1981; Michener
1983, 1984, Blumstein and Armitage 1998). Activity periods, annual cycles of body mass
and behavior may be subject to evolutionary pressures due to rapid changes in the
environment due to human disturbance, habitat destruction and environmental change.
The primary strategy of desert animals is avoidance of environmental extremes to reduce
energetic needs (Stiminski 2000). Therefore, an increase in variability or extremes may impact daily and seasonal activity patterns, annual cycles of body mass and activity cycles. Future studies across southwestern North America should focus on the influence of seasonal variation in temperature and precipitation on timing of activity periods, annual cycles of body mass, and time budget of behaviors, particularly for species of conservation concern (Ball et al. 2005; 2010).
ACKNOWLEDGMENTS
We would like to thank S. Blount, N. Cudworth, S. Ketcham, M. Levy, W.
Matter, G. McPherson, M. Merrick, E. Posthumus, and R. Steidl for comments on earlier
drafts that greatly improved this manuscript. Assistance in the field by B. Pasch was
greatly appreciated. Great thanks to the staff and volunteers at the Casa Grande Ruins
National Monument for access to sites and assistance. Funding was provided by the
Western National Parks Association, T&E Incorporation Conservation Biology Research
Grant, American Society of Mammalogists Grants-in-Aid Award, the Wildlife 53
Foundation Scholarship, Sigma Xi Grant-in-Aid of Research, and the Alton A. Lindsey
Award and Grant. 54
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Table 1.
Behaviors used in time budget analysis of round-tailed ground squirrels
(Xerospermophilus tereticaudus) at the Casa Grande Ruins National Monument, Pinal
Co., Arizona (2004-2007). References: aBalph and Stokes 1963, bDunford 1975.
Behavior Description
Resting, lying down not engaged in Basking any other activitya Either collecting dried grass or Collecting nest material running with a mouthful to burrowb Digging with fore feet first followed Digging by hind feeta, b Drumming of hind feet in rapid Foot drumming successionb Walking with nose to the ground; Foraging eating (jaws moving) b Direct interaction with another Social behavior individualb Locomotion, walking or running Traveling with nothing in mouthb
Vigilant Standing upright on hind feeta
73
Table 2.
Annual cycles of behavior in round-tailed ground squirrels (Xerospermophilus tereticaudus) at the Casa Grande Ruins National Monument, Pinal Co., Arizona (2004-
2007) including litter size ± SE, dates of initial emergence from hibernation of males and females, median estrus based on back calculation from litter emergence, and initial and final observation of initial emergence of litters, and last capture date for males and females.
2004 2005 2006 2007
Date of emergence 6-February 9-February 11-February 27-January (Adult male) Date of emergence 13-February 13-February 16-February 1-February (Adult female)
Median date of estrus 28-February 4-March 2-April 26-March
Date of initial litter 22-April 30-April 26-May 16-May emergence Date of final litter 2-May 10-May 9-Jun 29-May emergence Last date of capture 4-June 27-Aug -- 6-May (Adult male) Last date of capture 29-July 27-Aug -- -- (Adult female)
Litter size 4.6 ± 0.6 6.2 ± 0.4 4.8 ± 0.4 3.2 ± 0.4
74
Table 3.
Rankings of the top five models using Akaike’s Information Criterion with a small sample size correction (AICc) in Program MARK to explain the survival (phi) and detection probability (p) of round-tailed ground squirrels (Xerospermophilus tereticaudus) at the Casa Grande Ruins National Monument, Pinal Co., Arizona (2004-
2007).
Number of Model AIC Delta AIC Deviance c c Parameters
Phi(t) p(g) 693.0178 0.0000 28 278.4151
Phi(t) p(.) 701.5695 8.5517 27 289.3212
Phi(g*t) p(g) 718.7139 25.6961 52 242.9752
Phi(g*t) p(.) 721.1097 28.0919 51 248.1099
Phi(t) p(t) 728.4893 35.4715 49 260.9137
75
Table 4.
Body mass of male and female round-tailed ground squirrels (Xerospermophilus tereticaudus) at the Casa Grande Ruins National Monument, Pinal Co., Arizona (2004-
2007).
Malesa Femalesa
Emergenceb 146.7 ± 6.6c 117.9 ± 5.4
Pre-matingb 145.8 ± 5.4 130.0 ± 3.3 2004 Gestation 156.0 ± 12.4 135.7 ± 8.6
Pre-hibernationb -- --
Emergenceb 155.6 ± 5.2 c 145.7 ± 10.0 d
Pre-mating -- -- 2005e, f Gestation 170.8 ± 8.1 161.7 ± 4.2
Pre-hibernationb 221.3 ± 13.9 187.5 ± 13.6d
Emergenceb 127.0 ± 9.0 103.3 ± 1.7d
Pre-matingb 136.6 ± 7.2 107.0 ± 11.0 2006f Gestation 144.2 ± 15.3 147.1 ± 4.2
Pre-hibernationb 185.0 ± 5.0 150.7 ± 8.8d
Emergenceb 140.0 ± 4.4 c 93.0 ± 7.0d
Pre-matingb 151.7 ± 6.0 115.0 ± 8.9 2007e, f Gestation 151.7 ± 6.0 151.3 ± 9.8
Pre-hibernationb 195.0 ± 0 162.5 ± 4.2d 76
Table 5.
Proportion of time spent in each behavior category by adult male and female round-tailed
ground squirrels (Xerospermophilus tereticaudus) at the Casa Grande Ruins National
Monument, Pinal Co., Arizona (2004-2007).
Behavior Females Males
Social 0.003 <0.001 (Amicable & Agonistic)
Digging 0.022 0.013
Collecting nest matter 0.022 0.015
Foot drumming 0.026 0.003
Traveling 0.090 0.099
Basking 0.200 0.207
Foraging 0.310 0.411
Vigilant 0.330 0.254 77
Table 6. A comparison of the annual body mass and activity periods of sciurids, including the average body mass, dates of emergence for males and females, the length of active period (in months), the increase in mass over the active period
(calculated from the difference in body mass at emergence and immergence into hibernation), the number of days from female emergence to the start of the mating season, length of mating season (in days), and time spent vigilant and foraging and mean annual precipitation (in mm). Symbols used: aestimated.
References: Callospermophilus saturatus: Kenagy et al. 1989; Trombulak 1988; Cynomys ludoviciaes: Hoogland 1995;
Loughry 1992; Ictidomys mexicanus: Schwanz 2006; Young and Jones 1982; I. tridecemlineatus: Clark 1971; McCarley 1966;
Streubel 1975; Streubel and Fitzgerald 1978; Marmota flaviventris: Blumstein et al. 2004; Frase and Hoffmann 1980;
Marmota marmota: Ferron 1996; Marmota monax: Grizzell 1955; Kwiecinski 1998; Sinha-Hikim et al. 1991; Marmota olympus: Barash 1973; Edelman 2003; O. beecheyi: Dobson and Davies 1986; Evans and Holdenried 1943; Holekamp and
Nunes 1989; Leger et al. 1983; Owings et al. 1979; Otospermophilus variegatus: Ortega 1991; Oaks et al. 1987; Poliocitellus franklinii: Krohne and Schramm 1994; Ostroff and Finck 2003; Spermophilus armatus: Balph 1984; Eshelman and
Sonnemann 2000; Hannon et al. 2006; Knopf and Balph 1977; Slade and Balph 1974; Spermophilus citellus: Millesi et al. 78
1998, 1999a,b; Spermophilus xanthoprymnus: Gür and Gür 2005; Yiğit et al. 1999; Urocitellus beldingi: Jenkins and Eshelman
1984; Morton 1975; Morton and Sherman 1978; Sherman and Morton 1984; Urocitellus columbianus: Betts 1976; Elliott and
Flinders 1991; Murie and Boag 1984; Murie and Harris 1978, 1982; Shaw 1920; Young 1990; Urocitellus elegans: Zegers
1981, 1984; Urocitellus parryii: Carl 1971; Hubbs and Boonstra 1997; Lacey et al. 1997; Urocitellus richardsonii: Michener
1979; Michener and Koeppl 1985; Davis and Murie 1985; Xerospermophilus mohavensis: Bartholomew and Hudson 1960, Best
1995; X. spilosoma: Streubel and Fitzgerald 1978; X. tereticaudus: Munroe and Koprowski 2011, this study.
Start Length Mass Mass Body Emergence Emergence Active of of % % Mean Species change change mass (M) (F) period mating mating vigilant foraging Precip (M) (F) season season
Arctic
Callospermophilus 200- 15 Mar- 27 Mar- 4.5-5.5 4.7% 25.9% 1-2 14 11-28% 238 saturatus 350 12 May 28 May
4000 Marmota - May May 3 6% 30% 650 marmota 8000 79
3000 Marmota - May May 4-5 <1 20 1-5% 26-37% 540 olympus 4000
Urocitellus 125- 22 Apr- 15 May – 3-5 75.6% 63.2% 4-6 14 42-72% 105 beldingi 550 17 May 1 Jun
Urocitellus 380- 13 Apr- 19-29 Apr 4-4.5 57% 50% 4 14 6-26% 49-86% 357 columbianus 800 26 Apr
Urocitellus 750- 17.5 - 7-17 Apr 17-20 Apr 4-5 34.1 3-4 14 252 parryii 850 24.1%
Urocitellus 200- 11 Feb- 7 Mar- 45- 72- 3-4.5 3-4 14-35 613 richardsonii 425 12 Mar 14 Apr 74% 95.2%
Desert
Ictidomys late Mar- 250 Mar 7 63.0% 66.9% 7-14 7-14 359 mexicanus early Apr
Xerospermophilus 70- 136- 136- 1 Feb 15 Feb 5-6 163 mohavensis 80 329% 329%
Xerospermophilus May May 6 150 15% 45.6% 676 spilosoma 80
Xerospermophilus 125- 27 Jan- 1 Feb- 39.3- 28.7- 25.4- 31- 4-6 9-40 13 244 tereticaudus 150 11 Feb 16 Feb 45.7% 74.7% 33% 41.1%
Temperate
Cynomys 700- n/a n/a 12 20.7% 18.9% 14-21 19-28% 62-74% 392 ludoviciaes 900
Ictidomys 110- 12 Mar- 12 Mar -13 11.6- 4-6.5 39% 39% 12-13 42.4-70% 884 tridecemlineatus 140 6 April Apr 12%
2800 Marmota 12 Apr- 12 Apr- - 4-7 14 1-15% 12-23% 502 flaviventris 13 May 13 May 3900 3500 Marmota 29 Jan- 62.5- 55.8- - 11 Feb 6.5 7-14 974 monax 2 Mar 66.7% 88.5% 3800
Otospermophilus 500- 15 Oct- 15 Nov – 7.3- 7-8 40.8% 32.7% 36 28.9-74% 645 beecheyi 800 15 Jun 1 July 18.6%
Otospermophilus 550- Mid Mar Late Mar 7 21.8% 31.5% 28-42 57 variegatus 850
Poliocitellus 500- 15 Apr- 30 Apr- 4-5 45.4% 22.2% 781 franklinii 950 31 May 30 May 81
Spermophilus 60- 55- 300 21 Apr 24 Apr 3 2-4 14-21 35-50% 25-35% 41 armatus 95% 78%
Spermophilus 200- 28 Mar- 1-16 Mar 4-6 39.6% 46.5% 3 3-4 643 citellus 400 25 Apr
Spermophilus 235- 4 Jan- 4 Jan- 15.7- 15.7- 5-6 <1 21 416 xanthoprymnus 490 16 Feb 16 Feb 60.7% 60.7%
Urocitellus 226- 27 Mar- 36.8- 33.6- 9-30 Mar 4 1-3 7 18-27% 36-39.3% 332 elegans 280 17 Apr 88.5% 59.7%
82
Figure 1.
Precipitation (in mm) at the Casa Grande Ruins National Monument, Pinal Co., Arizona
(2004-2007). Figure 1a shows the annual pattern of the bimodal distribution of
precipitation. Figure 1b is photos of the field site from March 2005 (a year of high
precipitation) and 2007 (a year of drought, photos by K. Munroe).
Figure 2.
Parameter estimates of survival probability (Φ) ± SE of round-tailed ground squirrels
(Xerospermophilus tereticaudus) at the Casa Grande Ruins National Monument, Pinal
Co., Arizona (2004-2007) from the top model in Program MARK based on Akaike’s
Information Criterion with a small sample size correction (AICc): Phi(t) p(g).
Figure 3.
Litter size of 65 litters of round-tailed ground squirrels (Xerospermophilus tereticaudus) at initial emergence above ground at the Casa Grande Ruins National Monument, Pinal
Co., Arizona (2004-2007). Open circles show litter sizes observed and closed circles show the mean (± SE) for each year.
Figure 4.
Seasonal patterns of body mass of adult male (fig. 3a) and female (fig. 3b) round-tailed
ground squirrels (Xerospermophilus tereticaudus) at the Casa Grande Ruins National
Monument, Pinal Co., Arizona (2004-2007) over 4 time intervals: emergence, pre- 83
mating, estrus/gestation, and pre-hibernation, and date of last female captured. The last male captured is represented by a solid line.
Figure 5.
Activity budget of adult round-tailed ground squirrels (Xerospermophilus tereticaudus) at
the Casa Grande Ruins National Monument, Pinal Co., Arizona (2004-2007). 84
Fig. 1a 90 2003-2004
2004-2005 80 2005-2006 2006-2007 70
60
50
40
Precipitation (mm) Precipitation 30
20
10
0 Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep 85
Fig. 1b
2005 Photo by K. Munroe
2007 Photo by K. Munroe 86
Fig 2.
1.1
1.0
0.9
0.8
0.7
0.6
0.5
0.4
Survival Probability 0.3
0.2
0.1
0.0
Jul Jul Jul Sep Feb Jun Feb Jun Feb Jun Feb Apr Apr Apr Apr Aug Aug Aug Mar Mar Mar Mar May May May May 2004 2005 2006 2007 87
Fig 3.
12
10
8
6
4
2 Litter size at initial emergence initial at size Litter 0 2003 2004 2005 2006 2007 Year 88
Fig. 4a) males
250
200
42004 150 52005
100 62006
Body mass (g) 72007
50
0 Emerge Pre- Estrus Pre-
mating hibernate Fig. 4b
250
200 42004 150 52005
100 62006
Body mass (g) 72007 50
0 Emerge Pre- Estrus Pre- mating hibernate 89
Fig. 5 1
0.9 Collect nest material 0.8 Footdrum
0.7 Social
0.6 Dig 0.5 Vigilant 0.4 Proportion of time Forage 0.3
0.2 Bask
0.1 Locomotion
0 Females Males 90
APPENDIX B.
SOCIALITY AND GENETIC STRUCTURE IN A POPULATION OF ROUND-
TAILED GROUND SQUIRRELS (XEROSPERMOPHILUS TERETICAUDUS):
MODEL SPECIES OR OUTLIER?
Munroe, K. E. and J. L. Koprowski
(In the format of the journal Behavioral Ecology)
91
Socioecology and genetic structure in a population of round-tailed ground squirrels
(Xerospermophilus tereticaudus): model species or outlier?
Karen E. Munroe and John L. Koprowski
Wildlife Conservation and Management, School of Natural Resources and the
Environment, 325 Biological Sciences East, The University of Arizona, Tucson, AZ 85721
520-490-8948
Abstract: Solitary individuals to interactive groups of highly related individuals to
eusociality represent the sociality spectrum. Ground-dwelling sciurids exhibit a
continuum of sociality and several models predict levels of sociality. Models of ground squirrel sociality predict round-tailed ground squirrels (Xerospermophilus tereticaudus) to be solitary; however, previous behavioral studies suggest round-tailed ground squirrels have a matrilineal social structure. Thus if behavioral observations are truly informative, round-tailed ground squirrels represent a unique outlier. To resolve this discrepancy between observed and predicted levels of sociality, we combined field behavioral observations with genetic analyses of population structure. We assessed levels of agonistic and amicable behaviors combined with fine-scale population genetic structure of round-tailed ground squirrels in a multi-year study in Arizona. Only 45 agonistic and
40 amicable interactions were observed between adults in over 137 hours of behavioral observations. Overall rates of agonistic or amicable interactions between adults was low 92
(≤0.69/hour), with no relationship between relatedness of individuals and rates of either amicable or agonistic interactions. Interactions between juvenile littermates were predominantly amicable. Population substructure was not evident with Bayesian analyses, global or pairwise FST values; average relatedness among females was not
different from males. However, in 2006, the year after a population reduction through
targeted animal elimination, a population bottleneck was detected with at least five of
seven loci. Contrary to previous behavioral studies, the population of round-tailed ground squirrels we studied, although aggregated spatially, did not exhibit high levels of social behavior nor subpopulation genetic structure. This suggests round-tailed ground squirrels may be behaviorally flexible in social structure. Analyses of the genetic relationships and sociality along a continuum, particularly within aggregates of individuals, may lead to insights into the origin and maintenance of social behaviors by elucidating the mechanisms by which intermediate social level aggregates are formed and maintained.
Introduction
Solitary individuals and integrated groups of highly related individuals represent two ends of the sociality spectrum (Lott 1984). Solitary individuals should either avoid conspecifics or behave neutrally or agonistically in interactions with conspecifics; whereas individuals living in groups should exhibit social behaviors that define and maintain relationships within the group (Lott 1984). Social behaviors include any interaction (i.e., altruistic, amicable, and agonistic) among members of a group of individuals of the same species (Slobodchikoff and Shields 1988) that maintains group 93 structure. Intermediate levels of grouping (i.e., aggregates of individuals) occur in many species, yet are poorly understood, particularly levels of genetic relatedness among individuals and the presence and function of social behaviors (Lott 1991).
Three levels of hypotheses have been proposed to explain the origin of group formation: phylogenetic constraint, ecological (i.e., environmental) selection, and genetic
(i.e., kin selection, Slobodchikoff and Shields 1988). Each hypothesis proposes a different mechanism for group formation, but many of the benefits of social organization and behaviors remain the same. Behaviors costly to solitary individuals could be maintained within groups of highly-related individuals (Hamilton 1964; Alexander 1974;
Sherman 1981) by reducing costs of intraspecific competition (Bradbury and
Vehrencamp 1976; Wrangham and Rubenstein 1986) and parasite and disease transmission (Lott 1991) while increasing benefits of inclusive fitness of genetically related group members (i.e., kin selection, Hamilton 1964, 1972; Armitage 1981; Trivers
1985; Koenig and Mumme 1987; Emlen 1994, 1995). Genetic hypotheses predict that benefits of inclusive fitness create and maintain kin group formation (Hamilton 1964;
Alexander 1974; Armitage 1981; Koprowski 1996). Conversely, environmental selection dictates that environmental constraints (i.e., spatially and temporally heterogeneous resources and harsh climate) restrict individuals to coexist as aggregates as the cost of living solitarily are high. Determining whether kin or environmental selection is likely to have influenced the apparent aggregation of individuals can be resolved by examining genetic relatedness among individuals. In general, kin selection results in fine-scale genetic structure and groups of highly related individuals (i.e., kin clusters), whereas 94 environmental selection results in spatial aggregation without genetic structure within the population.
In mammals, female philopatry and male-biased dispersal produce and maintain clusters of related individuals that overlap in space and time (Greenwood 1980; Armitage
1981, 1999) and ultimately a population structure with subpopulations of related females
(Dobson et al. 1998; Sugg et al. 1996). This subpopulation structure has potentially important consequences for evolutionary processes, and creates further opportunities for kin selection (Cutrera et al. 2005), affects rate of inbreeding (Chesser 1991a, b; Sugg
1994), local adaptation (Storz 1999, 2005), and loss of genetic diversity (Melnick 1987;
Chesser et al. 1993; Sugg 1994; Dobson et al. 2004). Thus, the combined analysis of social behaviors and genetic relatedness of neighboring individuals within a population is an essential component in understanding the evolution of social structure and the origin of group formation. The ‘social structure’ view of population genetics, which incorporates analyses of subpopulation structure, dispersal rates and distances, mating strategies, and overall distribution of relatedness within a landscape (Chesser 1991a, b;
Lott 1991; Sugg et al. 1996) may be a useful tool to characterize how these factors co- vary and how social behaviors are maintained.
Ground-dwelling sciurids exhibit the continuum of sociality including several species with highly social behaviors (e.g., Olympic marmots, Marmota olympus: Barash
1973; Gunnison’s prairie dogs, Cynomys gunnisoni: Hoogland 1995) and species of isolated solitary individuals (Franklin’s ground squirrels, Poliocitellus franklinii, Iverson and Turner 1972; Murie 1973; woodchucks, M. monax, Maher 2009). Several models 95
have been proposed to describe the levels of sociality in ground squirrels (Armitage
1981; Michener 1983, 1984; Blumstein and Armitage 1998). The general model predicts
sociality in large-bodied ground squirrels (> 600 g, Armitage 1981) when juvenile and
adult activity periods overlap > 70% (Michener 1984) wherever adequate resources are
located. This pattern demonstrates social behaviors evolved to minimize aggressive and
competitive interactions due to the timing and sequence of the annual activity cycle
(Michener 1984), to improve care of young (Armitage 1981), increase efficient defense
of resources (Slobodchikoff 1984), and decrease predation risk (Blumstein and Armitage
1998). Understanding the genetic structure of ground-dwelling sciurid populations,
particularly species classified as intermediately social, should yield insights into the
nature of the evolution of social behavior within this group.
Round-tailed ground squirrels (Xerospermophilus tereticaudus) are small (~125 g) ground squirrels that inhabit desert areas of the southwestern United States including southeastern California, southern Nevada, and western Arizona, as well as northeastern
Baja California, and northwestern Sonora, Mexico (Hall 1981). Individuals are typically
active from late January to August at which time they enter an inactive phase or shallow torpor (Dunford 1975, Munroe and Koprowski in review). Males emerge first from burrows in late January, mating begins in early March (Ernest and Mares 1987), and young are born in late April to late June with lactation extending through June (Neal
1965, Munroe an Koprowski in review). Juvenile dispersal of 29-45% of young occurs during June and July (Dunford 1977a). Models of ground squirrel sociality predict round-
tailed ground squirrels to be solitary or form aggregates in favorable habitat based on 96 small body size, relatively long period of activity, and short period of adult-juvenile overlap (Armitage 1981). However, previous behavioral observations suggest round- tailed ground squirrels may have a greater social organization with a matrilineal population structure resulting in clusters of related females (Drabek 1973; Dunford
1977b), and high levels of social behavior, which would position round-tailed ground squirrels as a unique outlier in ground-dwelling sciurid sociality models. Patterns of social interactions differed between sexes and among age classes and vary significantly among seasons, but are most frequent between suspected kin (Dunford 1975; Dunford
1977b). However, little is known about the degree of relatedness within or between clusters of females within a population.
Round-tailed ground squirrels have been placed on both ends of the sociality spectrum. To resolve this discrepancy between observed and predicted levels of sociality and social organization, we combined field behavioral observations with genetic analyses to investigate the spatial genetic structure of two clusters of round-tailed ground squirrels and corroborate this with observed social behaviors. We predicted that, consistent with predictions of the ground squirrel sociality models, levels of social behavior and genetic relatedness of female round-tailed ground squirrels will be low. To test these predictions, we combined field data on observed rates of social behaviors analyses with genetic population structure.
97
Methods
We studied round-tailed ground squirrels at Casa Grande Ruins National
Monument in Coolidge, Pinal County, Arizona from January 2004 to June 2007.
Creosote bush (Larrea tridentata) dominated the landscape and was relatively evenly
dispersed with occasional barrel (Opuntia sp.), saguaro (Cereus giganteus) and planted ornamental cacti with trees around the visitors’ center and picnic area. Due to a large population size and potential damage to known and unexcavated archeological ruins, a population reduction though shooting and poisoning within the monument occurred during summer 2005, authorized by the National Park Service and performed by the U.S.
Department of Agriculture's Animal and Plant Health Inspection Service (APHIS). This reduction of the population provided an opportunity to monitor how population structure and social behaviors would change.
We established two 50-m2 study plots with a 50-m2 buffer area border at two
random locations within the monument (Figure 1). We used Sherman live traps (H.B.
Sherman Traps, Inc, Tallahassee, Florida) baited with sunflower seeds and/or peanut
butter to trap adult squirrels at burrows during the day. Squirrels were immobilized with a
cloth handling cone (Koprowski 2002) and all individuals were released at the point of
capture. We determined sex, and age class (juvenile < 6 mon, sub-adult 6-12 mon, adult
>12 mon) of squirrels upon initial capture after hibernation. We marked individuals with
a unique freeze-mark (Rood and Nellis 1980; Koprowski 1996) and hair dye (Clairol
Balsam Lasting Color, True Black #618, Procter & Gamble, Cincinnati, Ohio) for
permanent and immediate identification in the field. We used surgical scissors to collect a 98
4-mm2 tissue sample from the tail tip upon initial capture for genetic analysis. We stored
tissue samples in 1mL DMSO buffer solution at -20˚C upon exit from the field. Trapping
and handling were approved by The University of Arizona Institutional Animal Care and
Use Committee (IACUC number 07-026, 04-009) the Arizona Game and Fish
Department and the National Park Service.
Behavioral observations and analysis
We observed round-tailed ground squirrels during periods of daily activity from approximately 0600 to 1800 h. We used binoculars to observe behaviors from a distance of approximately 40 m. Scan samples were taken every 10 min to record any individuals present and focal animal observations were taken for 9 min to determine individual behavior and interaction rates (Altmann 1974). Quantified behaviors included frequency and classification (amicable or agonistic) of any physical contact with other individuals.
Amicable interactions included oral-oral and oral-nasal nuzzles. Agonistic interactions included chasing and lateral display, where two animals were side by side with their bodies and tails held low to the ground and their bodies were curved out, and these typically ended in a chase (i.e., “ready-alert”, Armitage 1962). Because animals did not always remain in view for the entire 9 min focal animal sample, we converted interactions to rates when appropriate. We combined the previously described interactions to create composite variables of amicable and agonistic behaviors.
DNA extraction and genotyping 99
We used standard phenol–chloroform methods (Sambrook and Russell 2001) with proteinase K, and a Tris-based cell lysis buffer to extract genomic DNA. We amplified seven polymorphic microsatellite DNA loci from other closely related species of ground squirrel (IGS-1, B-109, B-126, GS-12, GS-14, GS-25, GS-26; May et al. 1997, Stevens et al. 1997, Garner et al. 2005) with GoTaq polymerase (Promega Corp, Madison, WI) including a fluorescently labeled forward primer (6-FAM or HEX, IDT DNA
Technologies, IL, USA) and an unlabelled reverse primer. We conducted PCR amplifications in 25-µl volumes containing 50 ng genomic DNA, 1 µM each of fluorescently and non-fluorescently labeled primer, 0.2 mM of dNTP’s, 1.5 mM of
MgCl2, 5 ng BSA, 1X clear flexibuffer, 1U of GoTaq polymerase and 8.8 µl of PCR water. The thermal profile consisted of a denaturation cycle at 94oC (4 min); 35 cycles of
94oC (30 s) denaturation, 51oC (30 s) annealing, a 72oC (30 s) elongation; and a final extension at 72oC (5 min). We visualized PCR products on a 2% agarose gel to detect positive PCR. We performed post-PCR mixing before visualization on an ABI 3130
(Applied Biosystems, Foster City, California). Genotypes were visualized with
GENOTYPER software (v 3.7, Applied Biosystems, Foster City, California). We scored chromatogram data twice with two different observers to reduce scoring errors. We excluded individuals typed at fewer than five loci.
Data analysis
We used GENEPOP version 3.4 (Raymond and Rousset 1995) to calculate allele frequencies, allele number, observed Ho and expected He heterozygosities, and genotypic 100
linkage disequilibria. We used four approaches to investigate how genetic variation was
distributed within the population. All input file preparations were made using CONVERT
version 1.31 (Glaubitz 2004).
We used Bayesian assignment techniques to test for population structure using the
program STRUCTURE (version 2.3.2.1, Pritchard et al. 2000; Falush et al. 2003). This
method identifies genetically distinct clusters (K) of genetically similar individuals from
multilocus genotypes without prior knowledge of genetic relatedness incorporating the
likelihood of the data for different values of K. Since we expected only females in the
population to be philopatric (Drabek 1973; Dunford 1977b), we limited analyses to adult
females. We did not include juvenile offspring in our models because genetically distinct clusters tend to be overestimated when large groups of highly related individuals are included in the sample (Anderson and Dunham 2008). We ran STRUCTURE with and without the ‘admixture model’ option with 10 repetitions of 1,000,000 iterations following a burn-in period of 500,000 iterations. We assed data from each year
individually since only two females remained on the study plot between years. We used
HARVESTER to graph outputs from STRUCTURE. To determine the most likely
number of clusters, we used the method presented by Pritchard and Wen (2002), the
value of K that maximizes the estimated model averaged log-likelihood, log (P(X|K).
Recently, this method has been shown to perform as well as or better than the method presented by Evanno et al. (2005;Waples and Gaggiotti 2006).
We estimated population differentiation between study areas and among years in
ARLEQUIN version 3.1 (Excoffier et al. 2005). We calculated pairwise FST values using 101
methods outlined in Weir and Cockerham (1984). A Bonferroni correction for multiple
tests was used to determine significance of FST values among sampling locations and
years (Zar 1999). An analysis of molecular variance (AMOVA) was also calculated. We
used estimates of Wright’s (1931) F-statistics, FIS (genetic structure within localities),
and FST (among localities), to further investigate population differentiation by examining
the degree of genetic differentiation between our study areas and generated
corresponding 95% confidence intervals with FSTAT 2.9.3 (Goudet 1995). F-statistics
describe the amount of inbreeding-like effects within subpopulations FIS, among
subpopulations FST, and within the entire population FIT. The fixation index, or
differentiation coefficient of populations (FST), is used to evaluate the differentiation of
subpopulations. An FST value less than 0.05 denotes low differentiation between
subpopulations, 0.05 to 0.14 denotes a medium differentiation between subpopulations,
while an FST value of more than 0.15 means high differentiation between subpopulations.
FIS and FIT are inbreeding coefficients that give the probability of two identical alleles at
a locus being derived by descent from a common ancestor within the subpopulation (FIS) or from a common ancestor in the total population (FIT). Positive values of FIS and FIT
occur when there is increased homozygosity in a population including inbreeding and
mating system effects (Wright 1965; Nei 1977).
We used RE-RAT (Relatedness Estimation and Rarefaction Analysis Tool;
Schwacke et al. 2005) to calculate average relatedness for each group using the Queller and Goodnight (1989) relatedness estimator (R) based on Hamilton’s coefficient of relatedness, r. We calculated standard errors by performing a 10,000 jackknife re- 102 sampling procedure across all loci. Over all four years we calculated the overall relatedness for all males and females in the Monument and separately for each of the three years in the smaller study plots.
To test for the indication of a genetic bottleneck due to the target population reduction, we used the program BOTTLENECK version 1.2.02 (Cornuet and Luikart
1996; Piry et al. 1999) applying two mutation models: the stepwise-mutation model
(SMM), and two-phase model (TPM) of microsatellite mutation. The TPM combines the stepwise and infinite allele mutation models (Cornuet and Luikart 1996). We ran the
TPM analysis with the default setting of 70% stepwise mutation model and 30% variation from the infinite allele model (IAM). A total of 10,000 iterations were performed in each case. These models test whether observed gene diversity is higher than expected for mutation-drift equilibrium from the number of observed alleles in each locus. We performed one-tailed Wilcoxon-sign tests for heterozygote deficiency, indicative of a recent population bottleneck.
We used an analysis of variance (ANOVA) to test for a difference in the overall rates of amicable and agonistic interactions and linear regression to determine if rates of amicable or agonistic behavior were related with the genetic relatedness between pairs of adults and average relatedness within a litter of juveniles. We performed all analyses using JMP-IN (SAS Institute Inc. 2003). All means are reported ± SE.
103
Results
We captured and genotyped 351 unique round-tailed ground squirrels (98 adult females, 114 adult males, 51 juvenile females, 88 juvenile males) from February 2004 to
May 2007. Animals were aggregated on the landscape but dispersal and turnover rates do not support the formation of matrilineal kin clusters. Of the 40 adult females resident in the two 50-m2 study plots over the three years (2005: n = 18; 2006: n = 12; 2007: n = 10), only two females were present in consecutive years; one female showed natal philopatry
(2006) and one female immigrated into a plot, did not disperse after breeding, and did not produce a litter in the subsequent year.
Social behavior
Agonistic interactions included chasing and lateral displays; amicable interactions included oral-oral and oral-nasal nuzzles: Only 45 agonistic and 40 amicable interactions were observed between adults in more than 137 hours of behavioral observations
(Munroe and Koprowski in review) with one instance of burrow sharing. The ratio of agonistic to amicable interactions was 1.13:1. The overall rates of social behavior in adults were low (≤ 0.69/hour) and did not differ between years. No differences between rates of agonistic or amicable behavior between male-male, female-female, or male- female adult interactions (ANOVA, F6, 79 = 1.45, P = 0.21) were observed (Table 1,
Figure 2a, b). Agonistic (y = 0.006x + 0.053, t44= -0.22, P = 0.83; Figure 2a) and amicable interactions (y = 0.059x + 0.006x, t39 = -0.02, P = 0.99; Figure 2b) were not explained by level of relatedness for adult interactions. 104
For juveniles, we observed seven litters and a total of seven agonistic and 34 amicable interactions for a ratio of 0.21:1 agonistic to amicable interactions. The agonistic interactions were observed in a single litter of seven offspring during 2004. The level of amicable interactions was not explained by the average relatedness of the litter
(y= 1.79x + 0.28, t6 = 1.32, P = 0.24). No above ground interactions between mother and offspring were observed.
Population substructure
We detected 68 alleles at seven microsatellite loci with 4-18 alleles per locus. All loci had a low (< 0.039) frequency of null alleles and the absence of deviations from
Hardy-Weinberg equilibrium or patterns of linkage suggest that chosen loci were suitable for use in this study (for details see Table 2, Munroe and Koprowski 2011). Average relatedness of females within a group did not differ from males (z = 0.011, p > 0.99) or between groups within a year (2005: z = -0.012, n = 18, P > 0.99; 2006: z = -0.028, n =
12, P > 0.98; 2007: z = 0.003, n = 10, P>0.99; Figure 3). No population structuring was evident in this population, that the most likely number of clusters was one (K=1; Figure
4). Global FST values for each year and across years were less than 0.05 (Table 2).
However, global FIS among female residents was different from zero (Bonferroni corrected P = 0.001, Table 2). Pairwise FST values did not show subpopulation structure between plots or among years (Table 2). Most genetic variation (84%) in the population was due to differences within and among individuals (16%) and < 0.8% was explained between groups indicated by the AMOVA. 105
Bottleneck
In 2006, the year after population reduction, we detected evidence of a genetic bottleneck. In the two-phase model (TPM), where 70% of mutations are stepwise, a heterozygosity deficiency was detected in five of seven loci (Wilcoxon sign-rank, P =
0.11); however the stepwise-mutation model (SMM) detected a heterozygosity deficiency in six of seven loci (Wilcoxon sign-rank, P = 0.02). No deficiency in heterozygotes was detected by the TPM (2005: p = 0.82; 2007: P = 0.53) nor the SMM (2005: P = 0.07;
2007: P = 0.29) in the year prior to (2005) or after (2007) the population reduction.
Furthermore, detection of the change in heterozygosity suggests that the genetic power is sufficient to detect population substructure if present.
Discussion
Observation of social behaviors does not always infer a high degree of genetic relatedness among participants. Recently, evidence for the ecological hypothesis of group formation (Griffin and West 2002; West et al. 2002; Blundell et al. 2004; Matocq and
Lacey 2004; Hare and Murie 2007; Túnez et al. 2009) proposes models based on mutualism, reciprocal altruism and ecological advantages (i.e., access to a limited resource or predator avoidance, Connor 1995; Mesterton-Gibbons and Dugatkin 1992) can favor and maintain social behaviors. Rates of vigilant behavior in Columbian ground squirrels (U. columbianus) did not differ between kin groups or groups of unrelated members (Fairbanks and Dobson 2010). Social behaviors and tolerance of neighbors may 106
occur despite a group having a low relatedness (Trivers 1971; Wrangham 1982), which
may imply a high benefit-to-cost ratio for these associations and behaviors. Social
behaviors of ground squirrels may be directed toward maximizing direct fitness instead of
indirect fitness (Hamilton 1964; Armitage 1988) and therefore kin selection would not be
necessary to explain the frequency of social behaviors.
The population of round-tailed ground squirrels we studied, although aggregated
spatially, do not appear to be social on our study area. Round-tailed ground squirrels were
previously thought to be outliers in the ground-squirrel sociality models based on observations of social behaviors (i.e., approaching and withdrawing from conspecifics, oral-oral and oral-nasal nuzzles) of marked animals (Dunford 1977a). We would expect individuals living solitarily to be either neutral, avoidant or agonistic to each other and individuals living in groups should exhibit behaviors that maintain relationships within the group. Within our population of adult round-tailed ground squirrels, few social behaviors occur above ground but tolerance of individuals in the aggregate was common.
Overall rates of interactions between adults above ground were low and similar to other sciurid species, which range from 0.43 5.00 per hour (Wyoming ground squirrel: U. elegans, Zegers 1981; thirteen-lined ground squirrel: Ictidomys tridecemlineatus and spotted ground squirrel: X. spilosoma, Streubel 1975; Beldings ground squirrel: U. beldingi, Morton 1975; Columbian ground squirrel: U. columbianus, Betts 1976;
California ground squirrel: Otospermophilus beecheyi, Leger et al. 1983; Cynomys ludovicianus, Loughry 1992). Furthermore, occurrence of the population reduction and genetic bottleneck in our population of round-tailed ground squirrels did not disrupt rates 107
of social behavior. A reduction in population size can modify population structure and
rates of behavior (Meffert and Bryant 1990; Svobodová et al. 2011). An increase in
population size may lead to an increase in agonistic interactions (Butler 1980) and a
reduction in population size may lead to decreased agonistic and increased amicable
behavior due to a reduction in the number of possible roles (Blumstein and Armitage
1998). The rates of social behaviors did not change in our population after the bottleneck
further confirming the overall low level of sociality within the population.
The majority of interactions between juvenile littermates were amicable (83%)
with agonistic interactions only observed in a single litter. The percentage of those
interactions that were amicable is similar to other sciurid species, which range from
nearly 100% to 30% (Rayor and Armitage 1991). Neither amicable nor agonistic above
ground interactions between mother and offspring were observed. Typically mothers
exited a burrow to forage and juveniles emerged after the mother was away from the
burrow entrance. Social tolerance by adults towards young other than their own offspring
is a necessary step in the evolution of sociality (Lott 1984); we did not observe any
interactions between non-related adult and juveniles.
Our data demonstrate the importance of combining genetic and behavioral data as
so often behavioral data alone do not provide sufficient detail. Contrary to previous
studies (Drabek 1973; Dunford 1977b), but similar to the predictions of the models of
ground squirrel sociality (Armitage 1981; Michener 1983, 1984; Blumstein and Armitage
1998), female aggregates in our population of round-tailed ground squirrels were not highly related to each other and did not show subpopulation genetic structuring. Field 108
observations showed a 97% annual turnover rate for adult females and over 95% of female natal dispersal off the study plots. Mean coefficient of relatedness for aggregates
of females was neither different overall, between plots for all three years, nor compared
to relatedness among males. Bayesian analysis, global FST values for each year, and all
pairwise FST values between study plots and years further support the lack of population
substructure. Global FIS values differed from zero, suggesting probable inbreeding;
however, this may be due to the high degree of promiscuity and non-random mate choice
(Weir and Cockerham 1984; Cockerham and Weir 1987; Chesser 1991a) in this
population (Munroe and Koprowski 2011) and confounded with the effects of a recent
bottleneck due to target population reduction. Overall, these results suggest a lack of
genetic structure within this population, but not panmixia.
Female kin associations occur among several species of ground-dwelling
squirrels, including thirteen-lined ground squirrels (Vestal and McCarley 1984),
Belding’s ground squirrels (Sherman 1981), Richardson’s ground squirrels (U.
richardsonii, Michener 1979; van Staaden et al. 1996), Arctic ground squirrels (U.
parryii, McLean 1982), Columbian ground squirrels (Festa-Bianchet 1981; Harris and
Murie 1984), and probably in California ground squirrels (Owings et al. 1977), Uinta
ground squirrels (U. armatus, Slade and Balph 1974), black-tailed prairie dogs (Hoogland
1995), Gunnison’s prairie dogs (Hoogland 1995), Olympic marmots (Barash 1973),
hoary marmots (M. caligata, Barash 1974), and woodchucks (Maher 2009). However,
other ecological and environmental factors likely influence sociality in ground-dwelling
sciurids, including predation, the distribution and availability of resources in space and 109 time (i.e., food, burrows) and harsh environments (Crook 1972; Emlen and Oring 1977;
Ebensperger 2001; Armitage 2007; Hare and Murie 2007).
Spatial distribution and general abundance of food resources do appear to have been instrumental in the evolution of ground squirrel sociality. In Gunnison’s prairie dogs, social groups form in environments with patchy resource abundance
(Slobodchikoff 1984; Travis and Slobodchikoff 1993; Travis et al. 1995). In black-tailed prairie dogs, although nepotism has been noted, amicable and aggressive interactions also varied between seasons rather than with degree of relatedness (Hoogland 1986). Within our study area, food resources, including creosote bushes (Munroe and Kopwroski in review), were evenly distributed (Woodell et al. 1969) but varied temporally through extreme environmental conditions with high daily temperatures and extended droughts
(Munroe and Koprowski in review). Furthermore, predators on the site were common and included gopher snakes (Pituophis melanoleucus), Mohave rattlesnakes (Crotalus scutulatus), western diamondback rattlesnakes (C. atrox), burrowing owls (Athene cunicularia), great-horned owls (Bubo virginianus), Cooper’s hawks (Accipiter cooperii), red-tailed hawks (Buteo jamaicensis), badgers (Taxidea taxus), coyotes (Canis latrans) and feral dogs (C. familiaris). Differences in resource availability, both spatially and temporally, may lead to different levels of sociality within the species, possibly resulting in different levels of sociality observed in this study compared to the previous study by
Dunford (1975).
Under various ecological conditions, social organization may vary (Lott 1991); social and behavioral flexibility have been observed in Gunnison's prairie dogs (Travis et 110
al. 1995), raccoons (Mech and Turkowski 1966; Gehrt and Fritzell 1998; Ratnayeke et al.
2002), and woodchucks (Maher 2009, 2010). Round-tailed ground squirrels may have
behavioral flexibility in dispersal that leads to different levels of social organization
(Ratnayeke et al. 2002; Maher 2006; McEachern et al. 2007). Future research that
experimentally tests the influence of food and resource abundance, density, habitat
saturation, and density dependent factors leading to delayed dispersal and shared space
by female kin might help elucidate the proximate causation and ultimate benefits in this
species (Wolff 1993, 1994; Le Galliard et al. 2005).
The rigid definition of sociality and its association with genetic relatedness should
be modified to include alternative paths of group formation (i.e., ecological constraint
hypothesis), where all possible evolutionary costs and benefits of behaviors are
considered regardless of degree of relatedness within the group (Hare and Murie 2007).
Clustering of rodents may simply be due to high population densities rather than a stable
social organization with social relationships and behaviors (Randall 1994, 2008). High
densities, such as our population of round-tailed ground squirrels, may have the effect of
creating a single aggregate such that kin clusters are not able to form (Hamilton 1964;
Armitage 1975). Furthermore, social tolerance may be important for both social and solitary desert rodents because it minimizes the effects of physiological stress and water
loss (Randall 2008).
Comparative data from a continuum of kin-structured societies including low to
moderately kin-structured aggregates are important in order to delineate how social and
fine-scale genetic structures co-vary and may lead to insights about the evolution of 111
sociality in mammal populations (Dobson 1998). Social and genetic structure may be
more common in solitary species than previously considered (Ratnayeke et al. 2002;
Maher 2009) and therefore it is imperative to compare the fine-scale genetic structure with levels of social behaviors. Social behaviors of ground squirrels may be directed toward maximizing direct fitness (i.e., access to limiting resource, predator alarm calls) and not indirect fitness (Armitage 1988; Fairbanks and Dobson 2010); therefore kin selection would not be necessary to explain the frequency of these behaviors.
Furthermore, genetic and observational studies of intraspecific variation in spatial and social relationships may prove useful in resolving the conditions necessary for group formation, conditions that promote philopatry and kin-based sociality. Ultimately, analyses of genetic relationships within aggregates of individuals may lead to insights to the origin of social behaviors, and environmental conditions that may facilitate group formation and maintenance (Slobodchikoff and Shields 1988; Lacey 2000).
Acknowledgments
M. Levy generously provided laboratory space and equipment for genetic analyses. M. M. Levy, J. Busch, and A. Munguia-Vega provided genetic expertise and assistance. Additional laboratory equipment was provided by D. Zielinski. We would like to thank N. Cudworth, R. Jessen, T. Jessen, W. Matter, G. McPherson, M. Merrick, K.
Pelz-Serrano, R. Steidl and 2 anonymous reviewers for comments on earlier drafts that greatly improved this manuscript. Assistance in the field by B. Pasch was greatly 112
appreciated. Great thanks to the staff and volunteers at the Casa Grande Ruins National
Monument for assistance and access to sites. Funding was provided by the Western
National Parks Association, T&E Incorporation Conservation Biology Research Grant,
American Society of Mammalogists Grants-in-Aid Award, the Wildlife Foundation
Scholarship, Sigma Xi Grant-in-Aid of Research, and the Alton A. Lindsey Award and
Grant.
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Table 1.
Rates of agonistic and amicable interactions of round-tailed ground squirrels
(Xerospermophilus tereticaudus) at the Casa Grande Ruins National Monument, Pinal
Co., Arizona (2004-2007) for male-male, female-female, male-female dyads broken down by adults and juveniles. Sample size indicated in prentices.
Agonistic Amicable
Male-Male (adult) 0.04 (7) 0.05 (7)
Male-Male (juvenile) 0.03 (4) 0.02 (3)
Female-Female (adult) 0.04 (6) 0.07 (7)
Female-Female (juvenile) 0.02 (5) 0.05 (3)
Male-Female (adult) 0.06 (7) 0.06 (6)
Male-Female (juvenile) 0 0.01 (2)
127
Table 2.
F statistics (FST, FIT, FIS) a measure of genetic differentiation from the program FSTAT
for female round-tailed ground squirrels (Xerospermophilus tereticaudus) at the Casa
Grande Ruins National Monument, Pinal Co., Arizona, per year (2005-2007) and total
over all years ± SE.
Year FST FIT FIS
2005 0.021 ± 0.016 0.281 ± 0.086 0.266 ± 0.090
2006 -0.015 ± 0.024 0.239 ± 0.110 0.252 ± 0.116
2007 0.033 ± 0.033 0.190 ± 0.148 0.159 ± 0.133
Total -0.010 ± 0.008 0.215 ± 0.103 0.223 ± 0.103 128
Table 3.
Pairwise FST values of round-tailed ground squirrels (Xerospermophilus tereticaudus) at the Casa Grande Ruins National
Monument, Pinal Co., Arizona from the program ARELQUIN for each study plot per year. P-values from jackknifing procedure (10,000) are reported in parentheses.
Plot 1, 2007 Plot 2, 2007 Plot 1, 2006 Plot 2, 2006 Plot 1, 2005 Plot 2, 2005
Site 1, 2007 0
Site 2, 2007 -0.024 (0.59) 0
Site 1, 2006 0.079 (0.14) 0.010 (0.66) 0
Site 2, 2006 0.034 (0.22) 0.044 (0.10) 0.042 (0.37) 0
Site 1, 2005 -0.041 (0.99) 0.013 (0.75) 0.041 (0.57) -0.004 (0.94) 0
Site 2, 2005 0.016 (0.43) 0.006 (0.52) 0.025 (0.56) 0.050 (0.20) 0.018 (0.64) 0 129
Figure 1.
Study area for round-tailed ground squirrels (Xerospermophilus tereticaudus) at the Casa
Grande Ruins National Monument (CAGR), Pinal Co., Arizona (2004-2007). The smaller inner squares indicate the locations of two 50-m2 sub-plots and the outer larger squares
indicate the 50-m2 buffer areas used for this study during 2005-2007.
Figure 2.
Regression of pairwise relatedness of participants on rates of agonistic (2a) and amicable interactions (2b) of adult round-tailed ground squirrels (Xerospermophilus tereticaudus)
at the Casa Grande Ruins National Monument, Pinal Co., Arizona (2004-2007). Squares
represent male-male interactions, circles represent female-female interactions, and triangles represent male-female interactions.
Figure 3.
Estimates of mean relatedness (R) and standard error through standard jackknife procedure (10,000) as calculated by the program RE-RAT for all female round-tailed
ground squirrels (Xerospermophilus tereticaudus) in the population at the Casa Grande
National Ruins Monument, Pinal Co., Arizona over all four years (2004-2007), all males in the population over all four years, and subpopulation comparison for females in each of two plots for 2005-2007.
130
Figure 4.
Mean of estimated Ln probability (±SD) by the potential number of populations of round- tailed ground squirrels (Xerospermophilus tereticaudus) at the Casa Grande Ruins
National Monument, Pinal Co., Arizona (2005-2007) from the program STRUCTURE, the value of K that maximizes the estimated model averaged log-likelihood, log(P(X|K) indicates the number of clusters (Pritchard and Wen 2002).
131
Figure. 1.
132
Figure 2a. Male-Male
Female-Female
Male-Female 0.12
0.10
0.08
0.06
0.04
0.02
0.00 Interaction rate (per hour) (per Interaction rate
0.00 0.10 0.20 0.30 0.40 0.50 0.60 0.70 Pairwise relatedness
Figure 2b
0.12
0.10
0.08
0.06
0.04
0.02
Interaction rate (per hour) (per Interaction rate 0.00
0.00 0.10 0.20 0.30 0.40 0.50 0.60 0.70 Pairwise relatedness 133
Figure 3
0.25 ) SE
± 0.20 ,
0.15
0.10 Females 0.05 Males
0.00
-0.05 Average group relatedness (R Average relatedness group
-0.10 Total 2005 2006 2007 134
Figure 4
-600 (±SD)
-700
-800
probability -900
-1000
-1100
-1200
-1300
Mean of estimated Ln Ln estimated of Mean 0 1 2 3 4 5 6 K 135
APPENDIX C.
SOCIALITY, BATEMAN’S GRADIENTS, AND THE POLYGYNANDROUS
GENETIC MATING SYSTEM OF ROUND-TAILED GROUND SQUIRRELS
(XEROSPERMOPHILUS TERETICAUDUS).
Munroe, K. E. and J. L. Koprowski.
(In press Behavioral Ecology and Sociobiology) 136
Sociality, Bateman’s gradients and the polygynandrous genetic mating system of round-tailed ground squirrels (Xerospermophilus tereticaudus)
Karen E. Munroe and John L. Koprowski
Wildlife Conservation and Management, School of Natural Resources and the
Environment, 325 Biological Sciences East, The University of Arizona, Tucson, AZ 85721
520-490-8948
Abstract: Historically, most mammals have been classified as polygynous; although recent molecular evidence suggests that many mammals may be polygynandrous, particularly the ground-dwelling sciurids. We genotyped 351 round- tailed ground squirrels (Xerospermophilus tereticaudus) using seven microsatellite loci to determine paternity in 31 litters from 2004 to 2007. Polygyny was evident in all years except in 2007, when the population size was reduced. Multiple paternity occurred in the majority of litters (55%) with 2.5 ± 0.26 sires/litter (n = 31). Forty-nine percent of resident males (n = 114) sired offspring, and of males that sired offspring (n = 56) 27% sired young in multiple litters in a single breeding season. Litter size was positively correlated with the number of sires. Through an indirect analysis of paternity, we found
21 litters (68%) with an average relatedness of 0.5 or less. Males had a greater opportunity for sexual selection (Is = 1.60) than females (Is = 0.40); Bateman’s gradient was also greater in males (1.07 ± 0.04, n = 56) than females (0.82 ± 0.08, n = 31). The 137 mating system in round-tailed ground squirrels defined through genetic analyses and
Bateman’s gradients is polygynandrous compared to the previously suggested polygynous mating system as established by behavioral observations and fits within the predictions of the ground squirrel sociality models. Upon evaluating the predictions of the sociality models among sciurid species, we found a negative relationship between the level of sociality with litter size and the average percentage of multiple paternity within a litter. Thus, recent genetic information and reclassification of mating systems support the predictions of the ground-dwelling squirrel sociality models.
Keywords: Arizona . Microsatellites . Multiple paternity . Parentage analysis .
Polygynandry
Introduction:
Mating systems are defined by patterns of reproductive behaviors that are influenced by spatial and temporal distributions of reproductively receptive females.
Female aggregation affects the reproductive strategies of males, specifically their ability to acquire and monopolize mates (Bradbury and Vehrencamp 1977, Emlen and Oring
1977, Clutton-Brock 1989). In polygynous mating systems, ecological factors create aggregations of reproductive females where males are likely to succeed in monopolizing mating opportunities (Emlen and Oring 1977). However, where males are unable to monopolize mating opportunities, mating systems instead tend to be polygynandrous, where neither sex is restricted to a single mate within a breeding season (Emlen and 138
Oring 1977). The potential fitness benefits to females mating with multiple males in
polygynandrous systems include fertility assurance by reducing genetic incompatibility
(Zeh and Zeh 1996,1997, 2001; Jennions and Petrie 2000), increasing genetic diversity of
offspring (Loman et al. 1988, Ridley 1993, Jennions and Petrie 2000), and avoiding
aggressive behaviors from courting males (Jennions and Petrie 2000, Wolff and
Macdonald 2004). Furthermore, post-copulatory sexual selection may occur through sperm competition(Parker 1970) or cryptic female choice (Møller and Birkhead 1989,
Birkhead 2000).
Traditional observational studies of mating systems often focus on male behaviors
(Clutton-Brock 1989, Shuster and Wade 2003), particularly the ability of males to monopolize access to reproductive females or resources required for mating such as food or breeding sites (Emlen and Oring 1977). Mating systems were classically defined by the number of mates per male or per female (Fisher 1930) or the ratio of sexually
reproductive males to receptive females (Emlen and Oring 1977). However, descriptions
of behavioral interactions between males and females demonstrate that sex ratio or the
number of observed copulations may not be an accurate indicator of the mating system
(Kokko and Monaghan 2001, Kokko and Johnstone 2002, Simmons and Kvarnemo
2006).
Mating systems are directly related to the intensity of sexual selection (Emlen and
Oring 1977, Andersson 1994). With the current use of genetic methods to evaluate
mating systems, the relationship between mating success and offspring production can
elucidate the relative strength of sexual selection in males and females. Recently, 139
Bateman’s gradients have emerged as a method that allows the comparison of intensities
of sexual selection across species and taxa (Jones et al. 2002, Becher and Magurran
2003). The relationship can be estimated by calculating the slope of a regression line
relating fecundity (number of offspring produced) to mating success (number of mates).
A nonzero Bateman’s gradient supports that sexual selection is operating in the
precopulatory phase of sexual selection (Jones 2009).
These gradients can also be compared between the sexes within a species to
assess the opportunity for sexual selection and determine the mating system. For
example, if males have a steep Bateman’s gradient and females have a shallow gradient,
then sexual selection will be stronger in males, and the mating system is likely to be
polygynous. If females have a steep Bateman’s gradient and males a shallow gradient,
then sexual selection tends to be stronger in females, and the mating system is predicted
to be polyandrous. If both sexes have Bateman’s gradients close to zero, the mating
system may be monogamous. If both sexes have steep Bateman’s gradients, they may
both compete for mates, and the mating system may be polygynandrous.
Due to limited data on genetic outcomes of mating behaviors, polygyny was
historically recognized as the predominant mating system in mammals (Krebs and Davies
1993, Birkhead 2000, Storz et al. 2001). Redefining mammalian mating systems as
polygynandrous, however, is becoming more common and is currently recognized in 133
species, 33 families, and nine orders (Wolff and Macdonald 2004). Recently, through genetic analyses, a variety of species previously classified as polygynous have been reclassified as polygynandrous, including white-tailed deer (Odocoileus virginianus: 140
DeYoung et al. 2009), roe deer (Capreolus capreolus: Vanpé et al. 2009), spotted tailed quolls (Dasyurus maculate: Glen et al. 2009), multimammate rats (Mastomys natalensis:
Kennis et al. 2008), and raccoons (Procyon lotor: Nielsen and Nielsen 2007). Thus, continued detailed genetic investigations of mating systems may indicate that polygynandry is the rule rather than the exception (McEachern et al. 2009). Polygynous and polygynandrous mating systems have different evolutionary consequences. Relative to polygynandrous, polygynous mating systems increase genetic relatedness within groups and genetic differentiation among groups (Chesser et al.1993, Nunney 1993), reduce effective population size by decreasing the number of males represented in the gene pool (Sugg and Chesser 1994), and affect genetic variability and evolutionary potential (Valenzuela 2000). Furthermore, differences in genetic structure of the population can have important implications for our understanding of population viability, genetic microevolution (Sugg et al. 1996, Parker and Waite 1997), and the intensity of sexual selection (Reynolds 1996) since variance in reproductive success is an important variable in the strength of sexual selection (Wade 1979, Wade and Arnold 1980).
Although male reproductive success is typically constrained by the number of mates obtained (Bateman 1948), the link between mating tactics and reproductive success is more imperceptible in females and not easily observable (Jennions and Petrie 1997,
2000).
Ground-dwelling sciurids show a continuum of mating systems from monogamous (e.g., Olympic marmot, Marmota olympus: Allainé 2000) to highly polygynandrous (e.g., yellow-pine chipmunk, Tamias amoenus: Schulte-Hostedde et al. 141
2002, 2004). These mating systems typically correlate with the social organization of the species. Ground dwelling sciurids are also known for their continuum of social organization (Armitage 1981, Michener 1983; 1984, Blumstein and Armitage 1998), from solitary individuals (e.g., woodchucks, M. monax) to groups of individuals of different ages and sexes that share space and have markedly overlapping home ranges, and demonstrate cohesive behaviors such as communication (e.g., black-tailed prairie dogs, Cynomys ludovicianus). Sociality in ground squirrels has been correlated with a large body size, habitats with short growing or active seasons with adequate resources, a long period of adult/juvenile overlap, and high levels of predation; the effects of these characteristics are clearly seen in the specialized anti-predator behaviors of these animals
(e.g., vigilance and alarm calling; Armitage 1981, Michener 1984).
An index of sociality was created by Armitage (1981) using a multivariate analysis of life-history characteristics for 18 species of ground-dwelling sciurids. This sociality index has five categories: rank 1: essentially solitary individuals (e.g., Franklin’s ground squirrel, Poliocitellus franklinii), rank 2: species that aggregate yet live individually in a favorable habitat (e.g., thirteen-lined ground squirrel, Ictidomys tridecemlineatus), rank 3: a male defends a set of individual females within his territory
(e.g., arctic ground squirrel, Urocitellus parryii), rank 4: a male defends a harem where females share burrows (e.g., yellow-bellied marmots, Marmota flaviventris), and rank 5: multi-harem colonies (e.g., black-tailed prairie dogs; Table 1). This model predicts that no species with a mean minimum adult weight <600 g and a total active season of 5 months or greater will be social. The model has been modified to include the active 142
period of adult and juvenile overlap and again high social indices are seen in ground
squirrels where the coincidence of activity is greater than 70% between adult and juvenile
ground squirrels (Michener 1984). Thus, this model suggests that social behaviors have
evolved as a way to minimize aggressive and competitive interactions due to the timing
and sequencing of the annual activity cycle (Michener 1984). More recent models focus
on the consequences of social complexity rather than on the evolution of complexity and
the life-history characteristics needed to increase the number of potential roles that
individuals can play within the social network (Blumstein and Armitage 1998).
Most ground squirrel species are classified with a social index of rank 2 or 3
(species that aggregate yet live individually in a favorable habitat or a male defends a set
of individual females) and as polygynous (e.g., thirteen-lined ground squirrel;
Richardson’s ground squirrel, U. richardsonii; arctic ground squirrel; Idaho ground
squirrel, U. brunneus; and California ground squirrel, Otospermophilus beecheyi;
reviewed in Waterman 2007). However, due to the introduction of genetic and
computational methods, several species have been reclassified as polygynandrous due to
the high occurrence of multiple paternity in litters (e.g., Columbian ground squirrels, U. columbianus; Raveh et al. 2010; Table 1). Furthermore, the detection of multiple mating by females is expected to increase due to new genetic analyses of mating systems (Zeh and Zeh 2001). The established social organization models of ground-dwelling sciurids can be used to make predictions about the mating system and reproductive ecology for a species. 143
Discrepancies between the classification of social organization and mating system exist for some species. Based on the model incorporating life-history characteristics,
round-tailed ground squirrels, Xerospermophilus tereticaudus, a small-bodied ground
squirrel with a long active season, were predicted to be a rank 2 species that aggregates
yet lives individually in a favorable habitat. However, based on behavioral and spatial
observations in the field (Dunford1977a), round-tailed ground squirrels were classified as
a rank 4 species having a semi-colonial population structure with a polygynous mating
system (Dunford 1977a, Waterman 2007) and thus were considered to be an outlier in the
social organization model. The opportunity is high for multiple mating by both sexes of
round-tailed ground squirrels given a long breeding season (personal observation), a
relatively large average litter size (x = 6.5 young, range 1–12; Reynolds and Turkowski
1972), overall high densities of individuals (range 5.3–40 individuals/ha; Drabek 1970,
Dunford 1977b), and a predicted low level of sociality (Armitage 1981). Based on these
ecological factors, we expected to find a high degree of multiple mating by both males
and females in the genetic expression of the mating system as seen in other ground
squirrel species with a similar sociality model rank (rank 2, e.g., thirteen-lined ground squirrels).
In this study, we describe the overall genetic mating system of round-tailed ground squirrels in two ways. We used microsatellite DNA markers to determine the patterns of parentage with direct and indirect methods; we also calculated paternity in litters with more than three offspring where mothers were known (direct paternity) and calculated the average relatedness in all litters with more than two offspring (indirect 144
paternity). We compared morphological variables (e.g., body mass, left hind foot length,
femur length) and the timing of reproduction to the number of offspring produced to
explain differences in reproductive success. We calculated the opportunity of selection (I)
and opportunity for sexual selection (Is) for each sex and Bateman’s gradient (βss) to
assess the intensity of sexual selection. Lastly, we evaluate the ground squirrel social
organization models and reproductive ecology variables including the genetic mating
system in round-tailed ground squirrels and among sciurid species.
Materials and methods:
Study area and sampling
We studied round-tailed ground squirrels at Casa Grande Ruins National
Monument in Coolidge, Pinal County, Arizona, from January 2004 to June 2007. Round-
tailed ground squirrels are small, non-sexually dimorphic, non-territorial ground squirrels
that inhabit the desert areas of southwestern USA and northwestern Mexico (Hall 1981).
They hibernate for a portion of the year, emerging from their burrow in late January, and
are active until July (Dunford 1975). The breeding season is defined by the presence of
scrotal males from mid-February through late April and is influenced by the quantity and
temporal distribution of spring rainfall (Neal 1965, Reynolds and Turkowski 1972).
Based on spatial and behavioral observations, round-tailed ground squirrels are believed to form a female-based, semi-colonial population structure through the male-biased
dispersal of adults in February and juveniles in July (Drabek 1970, 1973; Dunford
1977a). 145
Creosote bushes (Larrea tridentata) dominated the landscape with occasional barrel (Opuntia sp.), saguaro (Cereus giganteus), and planted ornamental cacti and with trees around a visitors’ center and picnic area. Annual precipitation averaged at 225.9 ±
33.1 mm and average daily temperatures ranged between −4.7 ± 1.06°C and 46.0 ±
0.95°C from 2004 to 2007 (ncdc.noaa.gov). However, 2007 had an extreme drought with a late onset of spring rainfall.
We used Sherman live traps (H.B. Sherman Traps, Inc, Tallahassee, FL, USA) baited with sunflower seeds and/or peanut butter to trap adult squirrels at burrows during the day. We immobilized the squirrels with a cloth handling cone (Koprowski 2002) and released all individuals at the point of capture. Males emerge on average 2 weeks before females; we attempted to capture all individuals within 2 weeks of emergence from hibernation. Upon initial capture, we determined the sex, age class (juvenile <6 months, subadult 6–12 months, adult >12 months), and reproductive condition. To determine reproductive condition, we visually inspected the testis position (abdominal, inguinal, or scrotal) for males and visually inspected the teats to assess the degree of distension, alopecia, and pigmentation (Larsen and Taber 1980) and inspected the vulva to determine swelling indicative of estrus for females. We measured body mass (± 5 g) with a Pesola spring scale (Baar, Switzerland), left hind foot length (± 1 mm), femur length (± 1 mm), and testes length (± 1 mm, after the testis had fully descended). We marked the individuals with a unique freeze mark (Rood and Nellis 1980, Koprowski 1996) and hair dye (Clairol Balsam Lasting Color, True Black #618, Procter & Gamble, Cincinnati, OH,
USA) for permanent and immediate identification in the field. We used surgical scissors 146
to collect a 4-mm2 tissue sample from the tail tip upon initial capture for genetic analysis.
We stored the tissue samples in 1 mL DMSO buffer solution at −20°C upon exit from the
field.
We recorded litter size at emergence aboveground. To ensure that juveniles could
be assigned to a litter, we captured individuals by trapping at the target burrow with
Sherman live traps and with noosing (Medica et al. 1971, Lacey et al. 1997b, Larrucea
and Brussard 2007). To noose animals, we placed a loop of polyester string over burrow
entrances and sat 4 m away. When a juvenile came aboveground, we rapidly tightened
the noose around the abdomen. We are confident that we captured >90% of littermates
from each litter based upon the litter size counts at the first appearance of juveniles
aboveground. The University of Arizona Institutional Animal Care and Use Committee
(IACUC number 07-026, 04-009) approved the trapping and handling procedures and we
obtained trapping permits from the Arizona Game and Fish Department and National
Park Service.
DNA extraction and genotyping
We used standard phenol–chloroform methods (Sambrook and Russell 2001) with
proteinase K and a Tris-based cell lysis buffer to extract genomic DNA. We amplified
seven polymorphic microsatellite DNA loci from other closely related species of ground
squirrel (IGS-1, B-109, B-126, GS-12, GS-14, GS-25, GS-26; May et al. 1997, Stevens et
al. 1997, Garner et al. 2005) with GoTaq polymerase (Promega Corp, Madison, WI,
USA), with primer sets including a fluorescently labeled forward primer (6-FAM or 147
HEX, IDT DNA Technologies, IL, USA) and an unlabelled reverse primer (Table 1). We
conducted PCR amplifications in 25-μl volumes containing 50 ng genomic DNA, 1 μM
each of fluorescently and non-fluorescently labeled primer, 0.2 mM of dNTPs, 1.5 mM of
MgCl2, 5 ng BSA, 1X clear flexibuffer, 1 U of GoTaq polymerase, and 8.8 μl of PCR
water. The thermal profile consisted of a denaturation cycle at 94°C (4 min), 35 cycles of
94°C (30 s) denaturation, 51°C (30 s) annealing, a 72°C (30 s) elongation, and a final
extension at 72°C (5 min). We visualized the PCR products on a 2% agarose gel to detect
positive PCR. We performed post-PCR mixing before visualization on an ABI 3130
(Applied Biosystems, Foster City, CA, USA). The genotypes were visualized with
GENOTYPER software (v 3.7, Applied Biosystems, Foster City, CA, USA). We scored the chromatogram data twice with two different observers to alleviate scoring errors. We excluded individuals typed at fewer than five loci.
Paternity analyses
A direct analysis of paternity was possible because the suspected mothers were captured and identified at the burrow. For the indirect analysis of paternity, we calculated relatedness among offspring pairs within a litter to determine the average relatedness within a litter. We used GENEPOP 4.0 (Rousset 2008) to assess the characteristics of
microsatellites, and test Hardy–Weinberg equilibrium, null allele frequency, and
polymorphic information content (PIC), which refers to the value of a marker for
detecting polymorphism within a population that depends on a number of detectable
alleles and the distribution of their frequency (Rousset 2008; Table 2). 148
For direct paternity analysis, we incorporated genotypic data into CERVUS 3.03
(Marshall et al. 1998), which calculates the log-likelihood ratio scores to estimate the most likely father of each offspring in each litter based on available genotypes and allele frequencies in the population. Other methods may exclude the true parents if genotype errors are present or if the relatives are candidate parents (Marshall et al. 1998, Jones and
Ardren 2003, Wagner et al. 2006). We estimated the statistical confidence (delta[Δ]) for critical values at 80% and 95% confidence levels based on a computer simulation of paternity inference with allele frequencies from the study population from CERVUS simulations for 10,000 cycles and assumed that 75% of males in the population had been sampled and 75% of loci had been typed.
The genetic studies of mating systems are often limited by the number and variability of microsatellites used, number of potential parents captured, whether a single parent is known, and the number of litters sampled with more than or equal to three littermates (Bernatchez and Duchesne 2000). The failure to assign paternity with high confidence may simply be due to a deficiency of informa- tive loci. The seven loci that we used to determine paternity had a relatively high level of polymorphism, and PIC, and thus had a high combined probability of detecting multiple paternity within a litter (Table
2).
We used the program ML-RELATE (Kalinowski et al. 2007) to calculate the number of fathers/litter indirectly by calculating the average relatedness of littermates.
We imported allele frequencies from GENEPOP and ran each litter individually. We 149
averaged the relatedness of each pair of offspring in each litter to calculate the overall
average relatedness within a litter.
Statistical methods
We used regression to test if litter size was related to the number of sires/litter and
if body mass, left hind foot length, or femur length was related to reproductive success
and used ANOVA to examine relationships between testes size and reproductive success
in males. We calculated a correlation matrix for all reproductive ecology variables and
levels of sociality predicted by the sociality models (Armitage 1981, Koprowski 1998) in
Table 1. For correlation analysis, we used the median value for all the reported means of
reproductive ecology variables. We performed all analyses using JMP-IN (SAS Institute
Inc. 2003) and set alpha at 0.05 for statistical significance. All means are reported with
their associated standard error. To determine the opportunity for sexual selection, the
value of I for each sex was calculated as the ratio of the variance in offspring numbers,
2 VO, to the squared average in offspring numbers, O , among members of each sex;
2 2 I♂=VO♂/O♂ and I♀=VO♀/O♀ (Shuster and Wade 2003, Wade and Shuster 2005, Shuster
2008). The difference of the variance in relative fitness between the sexes, ΔI = (I♂−I♀),
determines the potential and to what degree the sexes will diverge because fitness
variance is proportional to selection intensity. We calculated Bateman’s gradient (βss) as the slope of the least-squares regression of reproductive success (minimum number of offspring) on mating success (minimum number of mates; Andersson and Iwasa 1996,
Jones et al. 2005, Jones 2009). We used ANCOVA to examine the interaction between 150
sex and reproductive success to test if there was a difference in Bateman’s gradient
between the sexes.
Results:
We captured and genotyped 351 unique individual round-tailed ground squirrels
(98 adult females, 114 adult males, 51 juvenile females, 88 juvenile males) from
February 2004to May 2007. We had over 95% turnover rate for both males and females
within our study area over all 4 years. All loci (n = 7) had a low (<0.039) frequency of
null alleles and were in Hardy–Weinberg equilibrium (Table 2). We sampled 38 litters
with a mean litter size of 4.1 ± 0.38 young/ litter (range, one to 13 young/litter); however,
only 31 litters met the criteria of unique mothers with more than or equal to three
offspring genotyped at more than or equal to five loci (2007, two litters; 2006, six litters;
2005, nine litters; 2004, 14 litters). The age of the adults is difficult to determine;
however, only one marked female of known age was able to produce litters in
consecutive years and the litter produced in the second year only consisted of one
offspring. Of the 31 litters, 55% showed multiple paternity. The power of CERVUS to assign paternity to individual offspring was moderate to high at high (68%) and relaxed
(89%) confidence levels (95% and 80%, respectively). For maternity, CERVUS assigned individual offspring at high (62%) and relaxed (96%) confidence levels (95% and 80%, respectively) and 86 offspring met the 95% average mother–offspring–father exclusion
probabilities positive log-likelihood ratios. The offspring not assigned to a father are
likely due to nonresident males that were not sampled. Litter size was normally 151
distributed and positively related to the number of fathers/litter (Pearson’s correlation
coefficient, N = 33, p = 0.83, P <0.001).
Of the 114 adult males captured, 49% (n = 56) sired at least one offspring and
27% (n = 15) sired offspring in multiple litters during a single breeding season. For males
that sired more than one litter (n = 15), 14 males sired young in two litters and one male
sired young in three litters. Twenty percent of breeding males (n = 11) sired offspring in
consecutive years; however, no males sired offspring in multiple litters in multiple years.
Litters averaged 2.5 ± 0.26 fathers/litter over all litters (range 1–7; Fig. 1). In females,
litter size was not related to body mass (X̅ = 158.2 g ± 10.0, t22 = 0.17, P = 0.87), left hind
foot length (X̅ = 32.4 mm ± 0.91, t22 = −0.21, P = 0.84), femur length (X̅ = 32.1 mm ±
0.96, t23 = −1.59, P = 0.13), or date of litter emergence (t37 = −0.51, P = 0.61). In males, the number of offspring was not related to left hind foot length (X̅ = 33.1 mm ± 0.68, t61 =
0.74, P = 0.46) or femur length (X̅ = 32.6 mm ± 0.99, t59 = −0.73, P = 0.47); however,
body mass showed a negative relationship to the number of offspring produced (X̅ =
161.7 ± 7.7, t60 = −2.43, P = 0.02). Testis size did not differ among males that did not sire young (X̅ = 18.6 mm ± 1.5), sired young in one litter (X̅ = 16.8 mm ± 1.0), or sired young
in multiple litters (X̅ = 18.5 mm ± 0.9, n = 44, ANOVA, F2, 40 = 0.0767, P = 0.96).
In our indirect analysis of paternity by calculating the average relatedness of
littermates using ML-RELATE, 21 litters (68%) had an average relatedness of <0.5,
indicating that littermates were less than half-siblings and implying multiple sires. Ten
litters (32%) had an average relatedness of <0.25, indicating high levels of multiple
paternity (Fig. 2). 152
Males (n = 56) had a considerably higher opportunity for sexual selection (Is =
1.60) than females (n = 31, Is = 0.40). The difference in the variance between the sexes in
relative fitness, ΔI= (I♂−I♀), was 0.99 (Table 3). Bateman’s gradient was positive and
different from zero in males (y = 1.01x −0.01, r = 0.92, t55 = 26.44, P < 0.001) and
females (y =0.81x+0.26, r = 0.72, t30= −10.2, P < 0.001) and was greater in males (1.01 ±
0.04) than females (0.81 ± 0.08: n = 87, ANCOVA, interaction term, F3, 85 =5.19, P =
0.024; Fig. 3).
When we examined the correlation matrix of the predicted levels of sociality to reproductive ecology variables from the sciurid species in Table 1, two relationships emerged. The index of sociality and litter size had a negative relationship (y =
−0.9850454x + 7.242, r = 0.35, t13 = −2.65, P = 0.02; Fig. 4). The index of sociality and average percentage of multiple paternity in a litter also showed a negative relationship (y
= −0.1455x + 0.9579, r = 0.34, t13 = −2.56, P = 0.02; Fig. 5).
Discussion:
Many small mammals have been classified as polygynous (Waterman 2007), but
current molecular techniques often provide additional information about the genetic
outcome of mating behaviors that can modify these classifications and influence how we
view mammalian mating systems. A diversity of mating systems within ground-dwelling sciurids has been elucidated through the genetic analyses of paternity. Black-tailed prairie dogs (Foltz and Hoogland 1981) and yellow-bellied marmots (Schwartz and
Armitage1980) are relatively monogamous and have little to no multiple paternity (<5%) 153
in litters. Extra-pair copulations have also been detected in the monogamous alpine
marmot (M. marmota: Goossens et al. 1998). California (Boellstorff et al. 1994) and
Richardson’s (Hare et al. 2004) ground squirrels show high levels of multiple paternity in
their litters and Columbian ground squirrels have a polygynandrous mating system where
both males and females are mating in multiple (Raveh et al. 2010). In 33 studies of
species in the family Sciuridae, 65% of females mated with more than one male
(Waterman 2007). Furthermore, sperm competition is known in Belding’s (Hanken and
Sherman 1981), thirteen-lined (Foltz and Schwagmeyer 1989), and arctic ground
squirrels (Lacey et al. 1997a). The prevalence of multiple female mating, sperm
competition, and multiple paternity within a litter of ground squirrels suggests that
females within this taxon play a big role in mate choice and mating strategies.
Round-tailed ground squirrels had a polygynandrous mating system during most years when evaluated with molecular genetics, contrary to their previous classification as polygynous (Dunford 1977a). Multiple mating occurred in both sexes and females had sired multiple litters in all years. Males produced offspring with multiple females in 3 of
4 years except during a drought in 2007 when an overall reduction in population size and reproductive levels occurred (Munroe and Koprowski, manuscript in preparation). Of successful males, 27% sired young in multiple litters and 20% were able to sire young in multiple years, suggesting that polygyny was a common mating strategy available to males in our population. The average relatedness of littermates further supports a polygynandry mating system for round-tailed ground squirrels. An indirect paternity analysis showed that 68% of litters had an average relatedness of <0.5, suggesting more 154 than or equal to two sires per litter, and 32% of litters had an average relatedness of
<0.25, suggesting even higher levels of multiple paternity. The behavior of mate guarding or prolonged copulation might benefit males and increase their siring success. The observation of copulatory plugs collected in the field (Munroe and Koprowski 2011) also suggests that the high intensity of mate competition among males combined with the high levels of multiple paternity suggests that sperm competition and cryptic female choice may also play a role in this mating system (Koprowski 1992).
Although not previously used to assess ground squirrels, Bateman’s gradients standardize the covariance between phenotype and fitness and provide a direct measure of how mating success relates to the number of offspring produced (Shuster 2009). The sex with a shallow Bateman’s gradient is likely to have reproduction limited by the number of offspring, whereas the sex with a steep Bateman’s gradient is limited by mating opportunities (Bateman 1948, Arnold and Duvall 1994, Jones 2009). Thus, a trait that increases mating success will have a positive selection differential only if Bateman’s gradient is positive. If pre-copulatory sexual selection arises as a consequence of competition for access to mates, then the currency of sexual selection should be the number of offspring produced or sired. The difference of the variance in relative fitness between the sexes (ΔI) determines whether and to what degree males and females will diverge phenotypically since fitness variance is proportional to the selection intensity. A positive ΔI for male round-tailed ground squirrel suggests that sexual selection is acting more strongly on males; this may be through pre-copulatory male–male competition for access to females, female mate choice, or post-copulatory mate guarding or sperm 155
competition. Male and female round-tailed ground squirrels have steep positive
Bateman’s gradients (Fig. 3), suggesting that sexual selection is acting upon both sexes
and indicating a polygynandrous mating system (Andersson and Iwasa 1996).
Additionally, Bateman’s gradient is steeper in males than females, suggesting that males
are more limited by their mating opportunities than females. Due to the steep Bateman’s
gradient, we expect a persistent directional selection on mating success and on any trait
correlated with mating success.
Litter size was not associated with female round-tailed ground squirrel’s body
size, mass, or timing of reproduction. However, females are likely limited by the number
of offspring they can produce and care for and possibly the number of sires. An increase
in male reproductive success was not associated with increased body size, mass, or testes
size. Only 79% of males were captured and weighed within 2 weeks after initial male
capture after exiting hibernation; there are several possible explanations of this
relationship, including the possibility of lower-quality males that were unable to compete with higher-quality males for mating opportunities However, we assume the negative relationship between male body size and the number of offspring produced to be related to reproductively active males forgoing foraging in order to increase the number of mating opportunities. Furthermore, males may have a single or suite of traits that females are using to make mating decisions, which differentially increases some male mating success. Among sciurid species, many tactics for increasing reproductive success are observed, and these may correlate with the sociality ranking of each species. A discernable trend exists in male mating order as an advantage in reproductive success in 156
ground squirrels. First, male mating advantage is seen in Belding’s (Hanken and Sherman
1981, Sherman 1989), thirteen-lined (Schwagmeyer and Foltz 1990), California
(Boellstorff et al. 1994), and arctic ground squirrels (Lacey et al. 1997a). In Columbian
ground squirrels, there is a strong first-male advantage in paternity that is tempered with
an increased number of mates, indicating that sperm competition plays a significant role
(Raveh et al. 2010). Idaho ground squirrels are the exception, exhibiting last-male mating
advantage with 66–100% of offspring attributed to the last male to mate with the female
(Sherman 1989).
Traditional alternative mating tactics (e.g., satellite males) to increase
reproductive success have not been observed in ground squirrels (Raveh et al. 2010).
Although paternal care is not common in non-monogamous mammals (Clutton-Brock
1991), male European ground squirrels (Spermophilus citellus) with a lower mating
success provided parental care through digging and maintenance of natal burrows
associated with potential offspring, which led to an increase in litter mass at emergence
(Huber et al. 2002). Thus, reproductive success may also be increased through parental care. Additionally, yellow-bellied, alpine, and hoary marmots (M. caligata) show
behavioral plasticity in their mating systems based on the population density and
distribution of individuals (Holmes 1984, Armitage 1986, Kyle et al. 2007).
The established social organization models of ground dwelling sciurids can be
used to make predictions about the mating system and reproductive ecology for a species.
The correlation between social structure and litter size (Fig. 4) provides further evidence
for the social complexity model of Blumstein and Armitage (1998), where increased 157 social complexity is associated with smaller litter sizes, indicating that sociality has costs in terms of fewer offspring produced per reproductive bout. Sociality has evolved in ground squirrel species with large body size as a way to minimize aggressive and competitive interactions due to the timing and sequencing of the short annual activity cycle (Armitage 1981, Michener 1983; 1984). Therefore, the greater the number of offspring produced, the greater the amount of resource competition during that short active period, and with increased predation, parasite, and disease pressure the greater the predicted level of sociality (Armitage 1981, Michener 1983; 1984). However, an increased number of roles for individuals to fill (e.g., non-reproductive yearling) may provide benefits in future offspring survival.
Based on their social organization rank 2 (aggregates of individuals in a favorable habitat), we expected the round-tailed ground squirrels to have a mating system similar to those of Richardson’s, Belding’s, thirteen-lined, and Idaho ground squirrels. Our direct paternity analysis estimate of an average of 55% of multiple paternity in litters corresponds to the range of multiple paternity seen in those species (range 50–80%). We would also predict that a first male advantage would exist in this mating system based on its prevalence in similar species within this social organization and the presence of copulatory plugs (Munroe and Koprowski 2011); however, the number and order of males that each female is copulating with would be necessary to determine male mating strategy.
In relating the sociality models of ground-dwelling sciurids to their reproductive ecology and mating systems, we can see that the social systems not only impact the 158 genetic outcome of the mating system but also affect the genetic structure of the population. When comparing the levels of multiple paternity, there is a significant negative relationship between the level of social organization of a species and the average level of multiple paternity in a litter (Fig. 5). Species that are relatively asocial (rank 1–2) such as woodchucks, Belding’s, and Richardson’s ground squirrels have higher levels of multiple paternity in their litters, which tend to be larger in size at emergence.
Alternatively, highly social species tend to have lower levels of multiple paternity and smaller litter sizes. The variable of litter size obviously impacts the potential level of multiple paternity as smaller litter sizes lack the opportunity to show high levels of multiple paternity. However, this robust relationship is readily observed despite incomplete data (16 of the 45 species of sciurids). Furthermore, several estimates of litter paternity were calculated with allozyme and DNA fingerprinting data, both of which have a reduced ability to differentiate between individuals and reduce the estimate of multiple paternity in litters (I. tridecemlineatus: Schwagmeyer and Foltz 1990; O. beecheyi: Boellstorff et al. 1994; S. brunneus: Sherman 1989; U. beldingi: Hanken and
Sherman 1981; U. parryii: Lacey et al. 1997a; C. ludovicianus: Hoogland 1995; Sciurus carolinensis: David-Gray et al.1998). The inclusion of two species of tree squirrels further emphasizes the robustness of the sociality models (Koprowski 1998).
Incorporating additional samples from additional sciurid species with recent genetic techniques would most likely increase the explanatory power of the model.
Spatial and temporal distribution of resources and life-history tactics determine the social organization, which exerts a direct influence over the mating system (possibly 159
through reproductive skew), subsequent mating opportunities, genetic structure, and
ultimately differential individual ecological fitness within patterns of selection within
social groups (Ross 2001, Balloux and Lugon-Moulin 2002). However, the patterns of
social organization are not only single functions of ecological factors such as resource
distribution, risk of predation, and population density but are products of a subtly
interwoven relationship with several evolutionary outcomes such as mating systems.
Future studies that manipulate ecological factors or compare populations in habitats of
differing quality to determine their effects on sociality and reproductive success will
provide insights to the evolution of sciurid mating systems and will advance the understanding of the relationship between ecological patterns and dynamic reproductive strategies (Conrad et al. 2001).
Acknowledgments:
M. Levy generously provided laboratory space and equipment for genetic analyses. M. M. Levy and J. Busch provided genetic expertise and assistance. Additional laboratory equipment was provided by D. Zielinski. We would like to thank J. Baccus, N.
Cudworth, F. S. Dobson, R. N. Gwinn, R. Jessen, W. Matter, G. McPherson, M. Merrick,
R. Minor, K. Nicholson, B. Steidl, and three anonymous reviewers for comments on earlier drafts that greatly improved this manuscript. Assistance in the field by B. Pasch, particularly in noosing juveniles, was greatly appreciated. Great thanks to the staff and volunteers at the Casa Grande Ruins National Monument for access to sites and assistance. Funding was provided by the Western National Parks Association, T&E 160
Incorporation Conservation Biology Research Grant, American Society of Mammalogists
Grants-in-Aid Award, the Wildlife Foundation Scholarship, Sigma Xi Research Grant, and the Alton A. Lindsey Award and Grant. 161
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Table 1. A comparison of the reproductive traits of sciurids, including the average percentage of multiple paternity (n =
number of litters), the marker type used to make that estimate (A = allozyme, F = DNA fingerprinting, and M =
microsatellites), the average number of mates per female, the average litter size at emergence, the breeding season length
(measured in days), the estrus length (measured in hours), density (number of individuals/hectare), and a sociality index.
Measures of variance were included whenever possible. When estimates of paternity in litters were available from multiple
genetic techniques, we used the estimate from the analysis that had a higher probability of paternity elimination (e.g.,
microsatellite versus allozyme data). The sociality index is taken from Armitage (1981) for ground sciurids and Koprowski
(1998) for tree squirrels. Symbols used: aSD, b66-100% of juveniles were sired by the last male to guard a female (Sherman
1989), cBased on female nest burrow density, dfrom observation in the field, ecalculated from table 1 (Kyle et al. 2007),
festimated.
References: I. tridecemlineatus: Rongstad 1965, Mitchell 1972, Streuble and Fitzgerald 1978, Schwagmeyer and Wootner
1985, Foltz and Schwagmeyer 1989, Schwagmeyer and Foltz 1990; O. beecheyi: Boellstorff et al. 1994; Spermophilus
brunneus: Sherman 1989; Urocitellus beldingi: Sauer, 1976, Morton and Sherman 1978, Hanken and Sherman 1981,
Holekamp 1983, Sherman and Morton 1979; U. columbianus: Shaw 1920, Boag and Murie 1981, Murie and Harris 1982,
Dobson and Kjelgaard 1985, Elliott and Flinders 1991, Murie 1995, Raveh et al. 2010; U. parryii: Carl 1971, Hubbs and 177
Boonstra 1997, Lacey et al. 1997a; U. richardsonii: Wehrell 1973, Michener and Michener 1973, Michener 1980, Davis, 1982,
Hare 2004; X. tereticaudus: Drabek 1970, Reynolds and Turkowski 1972, Dunford 1977b; Cynomys gunnisoni: Travis et al.
1996, Hoogland 1997; 1999, Haynie et al. 2003; C. ludoviciaes: Hoogland 1995; C. parvidens: Haynie et al. 2003; M. caligata:
Barash 1989a, b, Kyle et al. 2007; M. monax: Grizzell 1955, Snyder and Christian 1960, Sinha-Hikim et al. 1991, Maher and
Duron 2010; M. marmota: Allainé et al. 1998, Goossens et al. 1998, Cohas et al. 2008; S. carolinensis: Brown and Yeager
1945, Thompson, 1977, Koprowski 1994, David-Gray et al. 1998; Tamiasciurus hudsonicus: Gurnell 1987, Lane et al. 2008
Average Breedin percentage of Average Average Estrus Sociality Species Marker g season Density multiple mates/female litter size length index length paternity
Ictidomys 2.3 ± 0.9a,d 6.2 ± 1.4 6.8 50% (n=16) A 12 13 4 5 2.5 18 2 tridecemlineatus 2.46 ± 0.96a,d ± 0.3 a Otospermophilus 6.67 ± 89% (n=9) A 6.7 ± 1.4a, d 7.1 ± 1.8 a 48 70.4 2 beecheyi 3.18 Spermophilus Unknownb A 1.3d 5.2 ± 1.4 12 13 4-6 2 – 14c 2 brunneus 4.7 ± Urocitellus beldingi 78% (n=38) A 2.7 3.3d 4.42 ± 2.06 14 1.2 304 2 0.3 57.8% 2.36 ± 0.55a - 2.1 ± 0.09 11.6 U. columbianus M 21 5 7 4 (n=147) 4.35 ± 0.17d, 5.4 61.7 178
4.1 ± 1.2 a 1.7 ± U. parryii 6% (n=16) F 1.9 ± 0.8d 14 6 3 6.1 0.3 3.0 ± U. richardsonii 80% (n=15) M 2.1 ± 0.1 3.8 5.2 21 35 1.4 27 2 2.3 Xerospermophilus 4.1 ± 0.38 12.75 ± 55% (n=33) M 2.5 ± 0.26 5.3 40 2 tereticaudus 6.5 3.6 61% (n=21); Cynomys gunnisoni M 2.05 ± 0.98a 2.91 ± 0.14 60 24 20 85 3 77% (n=44)
C. ludovicianus 3% (n=273) A 1.39 ± 0.61a 3.08 ± 1.06 a 14-21 < 24 10 35 5
C. parvidens 71% (n=14) M 3.95 ± 0.26 2.5 74 3
Marmota caligata 58% (n=33) M 3.12e 3
18.1 ± M. monax 63% (n=26) M 1.8 2.6 7 14 1 2.1 31.4 (n=34); 3.57 ± 0.48 M. marmota 19.4 ± 3.9 M 3 4.31 ± 0.17 (n=103) Tamiasciurus 71% (n=38) M 5.8 ± 0.3 3.0 ± 0.1 < 24 0.3 2 3.25 hudsonicus
Sciurus carolinensis 31%f (n=5) F 3.47 ± 2.12d 1.8 3.7 60 < 8 3 16 3.25
179
Table 2. Summary statistics from seven microsatellite loci used for a study of round-tailed ground squirrels (X. tereticaudus) at Casa Grande Ruins National Monument, Pinal Co., Arizona (2004–2007) including species where microsatellite originated; repeated core sequences of thymine (T), guanine (G) cytosine (C), and adenine (A); allelic richness of microsatellites; range of allele sizes; observed (HO) and expected (HE) heterozygosity and Hardy–Weinberg equilib- rium (H–W); and Polymorphic Information Content PIC and null allele frequency. Species of origin:
CGS=Columbian ground squirrel, S. columbianus (Stevens et al. 1997); NIDGS=Northern Idaho ground squirrel, S. brunneus brunneus (May et al. 1997); SIDGS=Southern Idaho ground squirrel, S. brunneus endemicus (Garner et al. 2005).
Species Core Allelic Allele size Null allele Locus H H H-W PIC of origin repeats richness range (bp) o e frequency IGS-1 NIGS TG 10 80-98 0.734 0.744 NS 0.705 0.001 B-109 SIGS GA 12 209-231 0.834 0.835 NS 0.817 0.002 B-126 SIGS CA 12 168-190 0.769 0.813 NS 0.788 0.022 GS-12 CGS TG 6 145-147 0.655 0.623 NS 0.589 0.039 GS-14 CGS TG 6 224-234 0.712 0.736 NS 0.698 0.014 GS-25 CGS TG 18 123-151 0.678 0.758 NS 0.725 0.015 GS-26 CGS TG 4 111-117 0.333 0.332 NS 0.290 0.004 180
Table 3. Measure of the opportunity for sexual selection of male and female round-tailed ground squirrels (Xerospermophilus tereticaudus) at Casa Grande Ruins National Monument, Pinal Co., Arizona (2004-2007). Opportunity for selection (I) is
2 2 variance in reproductive success (σ rs) divided by mean reproductive success (X̅ rs ) squared. Opportunity for sexual selection
2 2 (Is) is variance in mating success (σ rs) divided by its mean (X̅ ms) squared. Standardized variance in reproductive success (Is)
describes the opportunity for sexual selection and indicates maximum strength of sexual selection acting in a population (Wade
1979, Wade and Arnold 1980). Bateman’s gradient (βss) measures transformation of variation in mating success into variation
in Darwinian fitness, as measured by least-squares regression of reproductive success on mating success.
2 2 Sex X̅ rs σ rs I X̅ ms σ ms Is βss (95% CI)
Male 0.78 0.98 1.60 0.75 0.93 1.65 1.01 (1.05-0.97)
Female 2.50 2.53 0.40 1.56 1.61 0.66 0.81 (0.89-0.73) 181
Fig. 1 Number of mates as determined by genotyped offspring for male (open bars, n=56) and female (filled bars, n=31) round-tailed ground squirrels (Xerospermophilus tereticaudus) at Casa Grande Ruins National Monument, Pinal Co., Arizona (2004-2007).
Fig. 2 Overall average relatedness with associated SE between littermates for each litter with >2 juveniles (n=31) for round-tailed ground squirrels (Xerospermophilus tereticaudus) at Casa Grande Ruins National Monument, Pinal Co., Arizona (2004-2007).
An average relatedness of 1 suggests identical twins in a litter of 2 young, an average relatedness of < 0.5 suggests at least 2 sires for that litter (n=21), and an average relatedness of < 0.25 suggest 3 or more sires/litter (n=10).
Fig. 3 Bateman’s gradient for round-tailed ground squirrels (Xerospermophilus tereticaudus) at Casa Grande Ruins National Monument, Pinal Co., Arizona (2004-2007).
Bateman’s gradient is caluculated as slope of the least squares regression of relative reproductive success on relative mating success. Females are represented as open squares and solid line; males are represented by solid circles and dashed line.
Fig. 4 The relationship between the level of sociality (sociality index, Armitage 1981,
Koprowski 1998) and the median average litter size for the sciurid species listed in Table
1. Sociality in sciurids ranges from solitary individuals (one) to multi-harem colonies
(five).
182
Fig. 5 The relationship between the level of sociality (sociality index, Armitage 1981,
Koprowski 1998) and the average percent of multiple paternity in litters for the sciurid species listed in Table 1. Sociality in sciurids ranges from solitary individuals (one) to multi-harem colonies (five). Paternity analyses were conducted with allozymes, DNA fingerprinting and micro 183
Fig. 1
Proportion of population
Number of mates 184
Fig. 2
1.5
1.25
1
0.75
Relatedness 0.5
0.25
0 L2_04 L2_04 L5_04 L4_04 L3_04 L1_04 L8_04 L6_04 L6_05 L1_05 L4_05 L9_05 L5_05 L2_05 L7_05 L5_06 L2_06 L6_06 L4_06 L1_06 L3_06 L2_07 L1_07 L12_05 L11_05 L12_04 L12_04 L14_04 L19_04 L15_04 L18_04 L11_04 L17_04 Litters by year 185
Fig. 3
6
5
4 success)
3
2 Number of offspring ( reproductive
1
0
0 1 2 3 4 5 6 Number of mates (mating success) 186
Fig. 4
8
7
6
5
4
3
2 Median average litter size litter average Median 1
0 0 1 2 3 4 5 Sociality index 187
Fig. 5
100 90 80 70 60 50 40 30 20 10
Average multiple paternity in litters (%) in litters Average paternity multiple 0 0 1 2 3 4 5 Sociality index