Sexual Selection in the American Goldfinch (Spinus tristis): Context-Dependent
Variation in Female Preference
Dissertation
Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy
in the Graduate School of The Ohio State University
By
Donella S. Bolen, M.S.
Graduate Program in Evolution, Ecology, and Organismal Biology
The Ohio State University
2019
Dissertation Committee:
Ian M. Hamilton, Advisor
J. Andrew Roberts, Advisor
Jacqueline Augustine
1
Copyrighted by
Donella S. Bolen
2019
2
Abstract
Females can vary in their mate choice decisions and this variability can play a key role in evolution by sexual selection. Variability in female preferences can affect the intensity and direction of selection on male sexual traits, as well as explain variation in male reproductive success. I looked at how consistency of female preference can vary for a male sexual trait, song length, and then examined context-dependent situations that may contribute to variation in female preferences. In Chapter 2, I assessed repeatability – a measure of among-individual variation – in preference for male song length in female
American goldfinches (Spinus tristis). I found no repeatability in preference for song length but did find an overall preference for shorter songs. I suggest that context, including the social environment, may be important in altering the expression of female preferences. In Chapter 3, I assessed how the choices of other females influence female preference. Mate choice copying, in which female preference for a male increases if he has been observed with other females, has been observed in several non-monogamous birds. However, it is unclear whether mate choice copying occurs in socially monogamous species where there are direct benefits from choosing an unmated male. I found evidence for mate choice copying and suggest that copying occurs when choosing extrapair mates. In Chapter 4, I examine how social relationships among females influence copying. A female may be more likely to copy another female if they are
ii familiar with one another due to shared environments and experiences. I found that females are more likely to copy familiar rather than unfamiliar females, which has not been shown in this context. The latter two chapters show that social context is a source of variation that can cause a female to alter her preferences. This suggests an important potential role of female-female social relationships on male reproductive success and the evolution of male characteristics.
iii
Acknowledgments
I wish to thank, first and foremost, my advisors, Ian Hamilton and Andy Roberts, without whom this never could have happened. Their patience, guidance, and generosity are something for which I will always be grateful. I also wish to thank my other committee member, Jackie Augustine, for her helpful comments and advice. I thank the animal behavior joint lab group at OSU for their feedback on early versions of this manuscript.
Thanks to Sandy Shew, Barb Shardy, Andy Jones, Keith Tarvin, and Doug Nelson and the Borror Laboratory of Bioacoustics for assisting with a variety of technical, equipment, and design issues. Heather Devine, Anne Sabol, Kirsten Cadmen, Craig
Miller, Samantha McGlone, Sarah Hamza, Molly Bobich, Brooke Nerderman, and
Shannon Kelley were invaluable in helping to care for captive birds. Katelyn Scott deserves special thanks as my research assistant. Thanks also to Chadwick Arboretum
North, Waterman Agriculture and Natural Resources Laboratory Complex, the Wilma H.
Schiermeier Olentangy River Wetland Research Park, Highbanks Metro Park, and The
Dawes Arboretum for access to their properties. The Macaulay Library at the Cornell
Lab of Ornithology and the Borror Laboratory of Bioacoustics provided acoustic recordings. Taxidermy services provided by McNamara’s Taxidermy Studio (Lima,
Ohio). This project was supported by funding from D. Nelson and the Borror Laboratory of Bioacoustics, and The Ohio State University Alumni Grants for Graduate Research
iv and Scholarship. Finally, I wish to thank Steve Chordas and Wayne Babcock for always being encouraging and supportive.
v
Vita
1993 …………………………………B.S. Accounting, The University of Akron
2002 …………………………………B.S. Zoology, The University of Akron
2003 – 2004 ………………………...Wild Animal Keeper, Akron Zoological Park
2006 – 2009 ………………………...Graduate Assistant, Biology Department,
John Carroll University
2011 ………………………………...M.S. Biology, John Carroll University
2009 – present ………………………Graduate Assistant, Department of Evolution,
Ecology, and Organismal Biology and the
Center for Life Sciences Education, The Ohio
State University
Fields of Study
Major Field: Evolution, Ecology, and Organismal Biology
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Table of Contents
Abstract ...... ii Acknowledgments...... iv Vita ...... vi List of Tables ...... ix List of Figures ...... x Chapter 1. INTRODUCTION ...... 1 Chapter 2. LACK OF REPEATABILITY OF FEMALE PREFERENCE FOR SONG LENGTH IN THE AMERICAN GOLDFINCH (SPINUS TRISTIS)...... 10 ABSTRACT ...... 10 INTRODUCTION ...... 11 METHODS ...... 15 RESULTS ...... 26 DISCUSSION ...... 31 Chapter 3. EVIDENCE FOR MATE CHOICE COPYING IN A SOCIALLY MONOGAMOUS SPECIES, THE AMERICAN GOLDFINCH (SPINUS TRISTIS) ..... 37 ABSTRACT ...... 37 INTRODUCTION ...... 38 METHODS ...... 41 RESULTS ...... 48 DISCUSSION ...... 54 SUPPLEMENTAL MATERIAL ...... 59 Chapter 4. FAMILIARITY AMONG FEMALES INCREASES MATE CHOICE COPYING IN THE AMERICAN GOLDFINCH (SPINUS TRISTIS) ...... 62 ABSTRACT ...... 62 INTRODUCTION ...... 63 METHODS ...... 67 vii
RESULTS ...... 74 DISCUSSION ...... 78 SUPPLEMENTAL MATERIAL ...... 81 Chapter 5. CONCLUSION ...... 83 LITERATURE CITED ...... 89
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List of Tables
Table 1 Single Measures Intraclass Correlation Coefficients (ICC) to examine repeatability of female choice for short or long song and repeatability of time spent in the center of the arena...... 27 Table 2 Estimated marginal means and 95% Wald confidence intervals from the main effects of the Generalized Estimating Equation. Means represent the probability of choosing the long song...... 30 Table 3 Model effects in the Generalized Estimating Equation used to examine the effects of female preference for short or long song. Subject variable is the individual female and within-subject variable is trial...... 30 Table 4 Generalized Estimating Equation to examine the effects of treatment, bird age, and trial order on the difference in the proportion of time spent with the less preferred male over time spent with either male from the pre-test phase to the post-test phase. Subject variable is the individual female and within-subject variable is the treatment. ... 49 Table 5 Generalized Estimating Equation to examine the effects of treatment, bird age, and trial order on the difference in the proportion of time spent with the less preferred male over time spent with either male from the pre-test phase to the post-test phase. Subject variable is the individual female and within-subject variable is the treatment. ... 76
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List of Figures
Figure 1 Top-down interior view of one of the traps used to catch birds. Visible are the tunnels and at the middle right is one of the “windows.” ...... 17 Figure 2 Schematic of the custom-built arena (~ 2.4 m L x 0.9 m W x 0.6 m H) used for preference trials. Floor and walls are solid; top has a wire mesh cover. Dark gray areas represent unused spaces. Brown bars are perches. Green and pink boxes represent water and food dishes, respectively. Speakers are placed on the floor just outside of the arena; there is a screen “window” in the arena wall just in front of the speakers to allow for sound transmission. Thin solid lines represent a wire mesh barrier that separates the models from the female. Thick dashed lines represent solid barriers that are raised through the top of the arena via remote pulleys to allow the female access to all areas including perches in front of the models. Models have additional lighting provided by desk lamps containing natural daylight LED bulbs suspended approximately two feet directly above the models at each end of the arena. An opaque curtain surrounded the entire arena. Speaker clipart from
x
Figure 7 The difference in the proportion of time spent with the less preferred male over time spent with either male from the pre-test phase to the post-test phase based on the treatment. Treatments are the bird (female goldfinch, male goldfinch, female house finch) observed with the less preferred male during the observation phase. N=20 for each treatment. Columns represent the mean. Error bars represent 95% CI. NS=not significant, *=significant at P<0.05, **=significant at P<0.000 (Generalized Estimating 2 Equation, main effect=treatment, Wald Χ 2=15.226, P<0.000)...... 50 Figure 8 The difference in the proportion of time spent with the less preferred male over time spent with either male from the pre-test phase to the post-test phase based on the treatment and age of the focal female. Treatments are the bird (female goldfinch, male goldfinch, female house finch) observed with the less preferred male during the observation phase. N=20 for each treatment. “Younger” females are those in their first breeding season (N=9); “older” females are those in their second or later breeding season (N=11). Columns represent the mean. Error bars represent 95% CI. **=significant at P<0.000 (Generalized Estimating Equation, interaction=treatment*bird age, Wald 2 Χ 2=16.065, P<0.000)...... 52 Figure 9 The difference in the proportion of time spent with the less preferred male over time spent with either male from the pre-test phase to the post-test phase based on the treatment and order of trials. Treatments are the bird (female goldfinch, male goldfinch, female house finch) observed with the less preferred male during the observation phase. N=20 for each treatment. Presentation of the treatments was randomized among females across trials. Columns represent the mean. Error bars represent 95% CI. *=significant at P<0.05 (Generalized Estimating Equation, interaction=treatment*trial order, Wald 2 Χ 4=38.246, P<0.000)...... 53 Figure 10 Diagram depicting the relationship between trial, phase, and treatment. Treatments took place during the observation phase of each trial. During the pre-test and post-test phases, both the more preferred and less preferred males are alone. Vertical bars within each box represent the separation of the 3 different areas of the arena – the center where the focal female is placed and the 2 ends of each side section of the arena where the models are located. F=familiar, UF=unfamiliar. ♂+ = the more preferred male, ♂- = the less preferred male...... 72 Figure 11 The difference in the proportion of time spent with the less preferred male over time spent with either male from the pre-test phase to the post-test phase based on the treatment. Treatment is the bird (familiar or unfamiliar female) observed with the less preferred male during the observation phase. N=24 for the familiar female treatment and N=23 for the unfamiliar female treatment. Columns represent the mean. Error bars represent 95% CI. *=significant at P<0.05 (Generalized Estimating Equation, main 2 effect=treatment, Wald Χ 1=4.210, P=0.040)...... 77 Figure 12 The relationship between the length of time (in days) that the observer- demonstrator pairs were housed together and the difference in the proportion of time spent with the less preferred male over time spent with either male from the pre-test phase to the post-test phase for the familiar female treatment. N=24. R2=0.003. Error bars represent 95% CI. (F1=0.069, P=0.795)...... 78
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Chapter 1. INTRODUCTION
Sexual selection is an important evolutionary process capable of opposing the forces of natural selection. Darwin’s (1871) theory of sexual selection states that the evolution of conspicuous sexual traits is the result of differences in reproductive success caused by competition over mates. Sexual selection has two main components, male-male competition and female choice, both of which can affect reproductive success and the expression of male traits.
In intrasexual selection, members of the same sex engage in contests for access to mates. The nature of the contests may select for weapons, conspicuous signals (e.g., status badges), or both
(Andersson 1994). In intersexual selection, mating success for one sex varies because of choice by the other. Females are usually the choosier sex due to their increased parental investment compared with males (Andersson 1994). Evolution of male sexual traits and differing reproductive success of males results as those males possessing the qualities that are most preferred by females pass on their genes to the next generation. Understanding variation in female choice and its associated behaviours are key to deciphering the complexity of mate choice decisions and how those decisions contribute to the evolution of male sexual traits.
Female choice is influenced by the constraints and costs associated with searching for mates as well as female preferences for traits (Andersson 1994). A female’s mate searching behaviour is limited in three ways. Time constraints limit the number of males that can be visited and judged. Searching should not take place beyond the last date that she could initiate breeding and still achieve maximum success (Janetos 1980). In the great reed warbler
1 (Acrocephalus arundinaceus), for example, due to a general reduction in reproductive success during the course of a season, each day of mate sampling results in the reduction of fledging success of 0.02 young (Bensch and Hasselquist 1992). Mobility constraints may limit a female’s ability to travel through the habitat or to locate available males. Environmental conditions, physical features of the habitat, and predation risk also add to mobility constraints (Janetos
1980). Memories of the locations and qualities of the males that have been visited, as well as how long those memories are retained, are additional constraints that will affect a female’s mate searching behaviour (Janetos 1980). Additional direct costs might include aggression from competing searchers, greater risk of disease transfer associated with increased sampling, and energy spent searching for and sampling males, which is energy lost to foraging and other activities (Real 1990). Opportunity costs may be incurred by females that reject a male that meets or falls just below an acceptable threshold and leave to continue sampling additional males. The risk is that she may not only fail to find a better alternative, but she may also find that upon her return, this male has died, emigrated, or is now mated to a rival female (Real
1990). This type of opportunity cost probably happens quite often, especially in species that have short breeding seasons or synchronized female settlement (Bensch and Hasselquist 1992).
Females may be able to reduce the costs of choice by using information gained from other females (social learning). Social learning occurs when animals acquire information about their environment by observing the behaviours of others (Coussi-Korbel and Fragaszy 1995). In the context of mate choice, social learning can result in mate choice copying, in which a female is more likely to choose a male as a mate if he has been observed with other females (Wade and
Pruett-Jones 1990). Copying others can reduce costs compared with acquiring information through asocial learning (Laland 2004). Thus, a female constrained by time may benefit by
2 choosing a mate that has already been evaluated and selected by others, even though she may have reduced benefits in the form of male parental care (Jennions and Petrie 1997). Mate assessment in this social context allows a female to consider information gathered from other females about potential mates, in addition to the information gathered by the individual female on her own.
Preferences for traits, in addition to mate searching constraints and costs, can influence female choice. Mating preferences are the inclination of individuals to mate with certain phenotypes over others (Jennions and Petrie 1997). Further, Jennions and Petrie (1997) subdivide mating preferences into two parts, preference functions and choosiness, distinguished as follows: they define preference functions as the order in which an individual ranks prospective mates, and they define choosiness as the effort or energy that an individual is prepared to invest in assessing mates, including the number sampled and the time spent evaluating each mate.
Many of the male sexual traits preferred by females are condition-dependent (called informative traits by Candolin 2003), meaning their expression varies with the overall health or quality of the male. Condition-dependent traits impose necessary costs on males and, thus, are honest signals that convey information about the quality of the males possessing them or the resources offered (Candolin 2003, Bradbury and Vehrencamp 2011). Condition-dependent traits can range from morphological features, to behavioural displays, to the performance of tasks such as constructing bowers and acquiring and defending good territories. Female preferences may also develop for uninformative traits that provide no information about male quality or direct benefits. Most common are signals that evolve to exploit pre-existing sensory biases in the receiver (Candolin 2003). For example, birds that forage for berries may develop a general preference for the colour red. A male with red plumage may then “exploit” this pre-existing
3 preference for red to attract a female even though his red plumage may be unrelated to his true condition. Attending to uninformative traits, however, may still benefit the female if the uninformative traits improve detection of other signals (Candolin 2003).
Direct and indirect selection processes can act on female preferences. Direct selection acts on preferences that increase the survival or fecundity of the female, such as preferences that select for males based on resources provided (e.g., territory quality, parental care). Key to the process is the existence of an honest signal of the male’s ability to provide the benefit (Bradbury and Vehrencamp 2011). Pleiotropy is another form of direct selection occurring when genes for traits that affect female survival or fecundity and that are subject to natural selection (e.g., foraging ability) also affect a female’s mating preferences (Kirkpatrick and Ryan 1991). In direct selection, both the male trait and the female preference can evolve to be exaggerated without the need for a genetic correlation between them. On the other hand, indirect selection requires a genetic correlation/covariance between the trait and the mating preference for that trait
(Kirkpatrick and Ryan 1991). Runaway selection (or Fisherian selection, Fisher 1930) is a type of indirect selection where females selecting mates based on a preference for an extreme trait will have offspring with both the genes for the preference from the mother and the genes for the trait from the father. As the preference for the trait becomes increasingly exaggerated, so does the trait. The “sexy sons” model describes a runaway process whereby females again prefer to mate with the males that possess the most extreme trait values, producing sons that will have inherited the father’s genes for the trait. Thus, the female benefits because her sons will be more preferred and will have higher mating success (Bradbury and Vehrencamp 2011). Runaway processes, however, are evolutionarily unstable and will end when the survival costs to the male of producing and maintaining the trait (which will be subject to natural selection pressures) are in
4 equilibrium with the sexually-selected mating advantage (Bradbury and Vehrencamp 2011).
There is no empirical evidence that true runaway selection has ever occurred in nature
(Kirkpatrick and Ryan 1991, Bradbury and Vehrencamp 2011). Though runaway selection is unlikely to occur by itself, it often co-occurs with other selection processes, given that they all begin with the expression of a preference for a particular male trait (Bradbury and Vehrencamp
2011). Another indirect process leading to the evolution of preferences is the ‘good genes’ hypothesis. The good genes model (or indicator model) predicts that by choosing a high quality male (e.g., a male displaying evidence of increased survivability, health, or disease resistance) as her mate, a female gains indirect benefits by passing on his superior genes to her offspring
(Kirkpatrick and Ryan 1991, Bradbury and Vehrencamp 2011).
Female choice and preferences can vary within and among individuals. For example, the traits that a female evaluates and uses to choose a social mate (who provides direct benefits) may be entirely different from those traits used to evaluate and choose an extrapair mate (who provides only genetic benefits). Female preferences can also vary based on context; for example, females sometimes show preference for unfamiliar males or novel male phenotypes. Studies
(e.g., Odeen and Moray 2008, Fanjul and Zenuto 2013) have demonstrated that females find unfamiliar males more attractive as mates. If so, a female’s preference for novel phenotypes will vary based on her own experiences and information about the distribution of male phenotypes in the population. This variability can play a key role in evolution by sexual selection because it can affect the intensity and direction of selection on male sexual traits (Gibson and Höglund
1992, Kirkpatrick and Dugatkin 1994), as well as explain variation in male reproductive success
(Wade and Pruett-Jones 1990). Understanding the role that variability in preference can play in
5 the evolution of a male sexual trait requires knowledge of the variability of that behaviour both within and among individual females (Boake 1989, Jennions and Petrie 1997).
I hypothesize that mate choice copying can lead to variation. Copier (or observer) females will differ in when they choose to copy (Laland 2004). For example, a female constrained by time may benefit by choosing a mate that has already been evaluated and selected by others. Similarly, a female that has lost a mate due to death or divorce may also find it advantageous to copy the mate choice of another. However, even females that may benefit from copying may choose instead to seek out an unpaired male, even if he may be of lower quality.
For the female, her choice of whether to copy may involve trade-offs between parental care and mate quality. Opportunities to copy may also vary such that not all females will have equal chances to make extraterritorial forays to observe the mate choices of other females or to observe copulations among existing pairs. Variation can also arise from copying in whom females choose to copy (Laland 2004). Some females may copy the mate choices of older or more experienced females (Dugatkin and Godin 1993) whereas others may choose to copy the choices of dominant females. Familiarity is another characteristic that may lead to variation in whom to copy. Familiar females, more likely to have shared environments and experiences (Laland
2004), may also have similar socially-acquired mate preferences.
To explore sources of variation in female preference and to understand the role that mate choice copying plays in generating variation in preference, I conducted a series of mate choice experiments using the American goldfinch (Spinus tristis). The American goldfinch was chosen as the study species for a variety of reasons. First, they are sexually and seasonally dimorphic with males expressing multiple conspicuous sexual traits, which vary among individuals and for which females are known to have preferences (Johnson et al. 1993). Second, male goldfinches
6 do not defend territories until after a pair bond has been formed (McGraw and Middleton 2009).
This means that territory and/or habitat quality will have no influence on female preference in a mate. Eliminating this potentially confounding factor aids in the examination of female preferences because mate selection will be based mostly (or entirely) on secondary sexual characteristics of the male. Third, they are mostly socially monogamous, which was a characteristic of interest for Chapter 3. And, finally, goldfinches are gregarious year-round and are not known to defend food sources nor breeding territories (McGraw and Middleton 2009).
This social nature of the species makes them well suited to a project exploring the roles of social influences on variation of female mating preferences.
In Chapter 2, I determined within and among-individual variation in female preference for the male sexual trait of song length by measuring repeatability. Repeatability is the ratio of among-individual variation to the total variation in preference for a given trait and provides an upper estimate of heritable variation between individuals (Boake 1989). I found high within- individual and low among-individual variation in preference for song length leading to a lack of repeatability. The lack of repeatability suggests that context may be important in the expression of female preferences. The remaining chapters explore how context-dependence in the form of mate choice copying influences female preference and variation in preference in this species.
In Chapter 3, I identified the extent to which female mating preferences are influenced by the apparent mate choice decisions of other females in goldfinches. While mate choice copying has been observed in several non-monogamous avian systems, whether females copy the mate choices of others in monogamous systems is unknown except for zebra finches where results have been mixed (Doucet et al. 2004; Swaddle et al. 2005; Drullion and Dubois 2008; Kniel et al. 2015a, 2015b). The costs of copying mate choice are high in monogamous species due to the
7 direct cost of loss of male parental care. I found that the difference in the proportion of time spent with a previously less preferred male increased more after having observed him with another female goldfinch relative to two controls. I interpret this as evidence for mate choice copying and propose that copying takes place when females are searching for extrapair mates but not a social mate.
In Chapter 4, I assessed how familiarity between two females influences the strength for mate choice copying. Familiar individuals are more likely to have spent time in each other’s presence and to have experienced similar environments than are unfamiliar individuals (Laland
2004). Thus, a female may be more likely to copy the mate choice of another female if they are familiar. In addition, females compete for mates for a variety of reasons (reviewed in Rosvall
2011). Female competition for mates is costly (Rosenqvist and Berglund 1992, Slagsvold and
Lifjeld 1994, Harris and Moore 2005), and familiarity may act to lessen these costs by, for example, reducing direct aggression. I found that time spent with a previously less preferred male increased more after he was observed with a familiar female rather than an unfamiliar female.
Sexual selection on male traits, influenced by female preference and choice, may depend heavily on characteristics of the physical and social environment. The female’s social environment might be one such context. In Chapters 3 and 4, I present results of experiments varying social contexts of choice and find strong influences of the behaviour of other females on apparent preferences. We should not overlook the potentially vital role that a female’s social life may play in the variability of preferences (Jennions and Petrie 1997, Westneat et al. 2000).
Because the evolution of male traits is influenced by female mate choice, the results of this study
8 suggest an important potential role of female-female social relationships on male reproductive success and the evolution of male characteristics.
9 Chapter 2. LACK OF REPEATABILITY OF FEMALE PREFERENCE FOR SONG LENGTH IN THE AMERICAN GOLDFINCH (SPINUS TRISTIS)
ABSTRACT
Females can vary in their mate choice decisions and this variability can play a key role in evolution by sexual selection. One method for assessing variation in female preference for male traits is to measure repeatability of mate choice decisions. We assessed repeatability of female preference for song length because song length has been shown to be an honest indicator of male quality. We predicted that repeatability would be high and that females would prefer longer songs. We used a two-choice experimental paradigm to assess variability across four trials designed to measure both within-individual and among-individual variation in preference. We found no repeatability in preference for song length but did find an overall preference for shorter songs. Several factors might have contributed to the lack of repeatability, including the experimental arena design, the motivational state of the females towards mating, and a strong side bias. Interestingly, we found very high repeatability of time spent in the center of the arena and suggest that this might also relate to the motivational state of the females. Preference for short songs has not previously been reported. We propose that this result might be due to the editing of the songs used for the choice trials and the possible creation of a supernormal stimulus. Lack of repeatability and, therefore, high within-individual variation indicates that preference for song length may be weak when measured as an independent trait. We suggest that context, including the social environment, may be important in altering the expression of female preferences.
10 INTRODUCTION
Females can vary in their mate choice decisions and this variability can play a key role in evolution by sexual selection. As variability in female preferences increases, directional selection on male ornaments will decrease as will the intensity of selection on those traits
(Jennions and Petrie 1997). For example, if susceptibility to costs of sampling varies among types of females and each type varies in their preferences, the direction of selection will change depending on which female type is less limited in their ability to choose. In addition to affecting the intensity and direction of selection on male sexual traits, variability in female preferences can explain variation in male reproductive success. The more a male’s trait deviates from the mean of the females’ preferences, the more likely the mating success of that male will be negatively impacted (Boake 1989). If the mean of the preference continuously varies, then which males will be more successful will also keep changing. Furthermore, for evolution of female preference to occur, there must be heritable variation among individuals.
Understanding the role that variability in female preference can play in evolution by sexual selection first requires some measure of how variability in female preference for that trait is partitioned (Jennions and Petrie 1997). The total variation for preference includes among- individual differences, within-individual differences, and other (error) effects.
Heritability is the ratio of additive genetic variation to the total variation in preference for a given trait and provides information about how a trait will respond to selection (Boake 1989).
Heritability measurements are rarely published despite the fact that they can provide insight into the genetic factors of behaviors that are important to selection (Jennions and Petrie 1997, Boake
1989). Reasons for this may be that breeding studies can be expensive and time-consuming and that heritability estimates are difficult to generate in field studies.
11 In contrast, repeatability, which is the ratio of among-individual variation (genetic and environmental) to the total variation in preference for a given trait, can be obtained fairly easily by making repeated observations of marked individuals (Boake 1989). High repeatability indicates that there is variation present for selection to act upon. Furthermore, repeatability measurements provide an estimate of the upper limits of heritability without having to perform intensive breeding experiments. If repeatability is high, estimates of heritability can be high or low. Heritability will be high if most of the genetic variation is additive and the amount of environmental variation in the preference for a given trait is low. Heritability will be low if most of the genetic variation is non-additive and environmental variation is high. Conversely, if repeatability is low, estimates of heritability will always be low.
Repeatability will be high if among-individual variation is large relative to within- individual variation and repeatability will be low if within-individual variation is large relative to among-individual variation; therefore, changes in either the within or among-individual components of variation can change repeatability estimates. Among-individual variation will tend to be low if individuals are consistent with each other in their assessment of males and within-individual variation is low when individuals are consistent in their choices over multiple observations. Female sand gobies (Pomatoschistus minutus) show repeatable preferences for male body size and nest elaborateness within, but not among, individuals (r=0.613, Lehtonen and
Lindström 2008). Similarly, female American toads (Bufo americanus) exhibit within, but not among, individual repeatability in their preferences for low dominant frequency of calls (r=0.42,
Howard and Young 1998). A study by Forstmeier and Birkhead (2004) on zebra finches
(Taeniopygia guttata) found low, but significant, repeatability for beak color (r=0.17, P=0.039), high song rate (r=0.24, P=0.014), and male aggressiveness (r=0.16, P=0.048). However, they
12 found no repeatability of an individual female’s preference for male attractiveness suggesting that preferences are weak and that there is little variation in male quality. Repeatability can also be low if there are strong environmental influences (e.g., temperature differences) (Boake 1989) or fluctuations in a female’s current condition (e.g., receptivity or motivation) (Jennions and
Petrie 1997), both of which contribute to the error component of the denominator.
Variation that is low both within and among individuals would suggest that preference for a trait is universal, and selection will reduce variation in that male trait (Murphy and Gerhardt
2000). Alternatively, variation that is low within but high among individuals would suggest that mate preferences are unique to individuals. For instance, some of the females in a population may be evaluating males based on one trait, while others are considering males based on a different trait. This variation in female preference among traits might explain how multiple redundant traits are maintained, and why multiple traits and multimodal signals evolved
(Candolin 2003). When variation is high both within and among individuals, selection will maintain or increase variation in the male trait (Murphy and Gerhardt 2000). This variation in preference may help to resolve the “lex paradox”, explaining how genetic variation in male traits is maintained despite strong female choice for a select number of males (Andersson 1994).
For the present study, we measured repeatability in female preference for song length, which is a male trait that is attended to by females when evaluating potential mates (Catchpole et al. 1986, Clayton and Prӧve 1989, Eens et al. 1991, Wasserman and Cigliano 1991, Nolan and
Hill 2004, Pasteau et al. 2009). Certain song features, such as song length, can be associated almost exclusively with intersexual encounters. For example, male great reed warblers sing a
“long song” type when attracting females, then immediately switch to a “short song” type upon pair formation (Catchpole 1983). Similarly, prior to pairing, male goldfinches sing long versions
13 of songs that can last for several minutes. These long continuous songs are often associated with courtship. Shorter versions of songs are sung after nesting territories have been established
(Stokes 1950).
We expected that females would show an overall preference for longer songs. Song length may signal to females the quality of a potential mate, such that longer songs indicate higher quality males. Song length is associated with age in European Starlings (Sturnus vulgaris). Male age can be an indicator of quality such that an older male has demonstrated superiority (e.g., disease resistance, intelligence, ability to find food, etc.) in surviving to an older age. In species where males provide parental care (such as starlings and goldfinches), a male’s age may also reflect a level of experience that should make him a better mate or parent. In female choice experiments, starling males with the longest song bout lengths were preferred by females significantly more often than males with either intermediate or short song bout lengths
(Eens et al. 1991). The length of song bouts was positively correlated with the age of the male.
Similar results have been found in other species, where extra-pair paternity is positively associated with longer strophe lengths and age in blue tits (Parus caeruleus: Kempenaers et al.
1997), and in great tits (Parus major), where males that sing longer strophes have increased survival, higher lifetime reproductive success, and are defined (along with the song traits of less drift and larger repertoires) as better singers (Lambrechts and Dhondt 1986).
To measure variation in preference for the male trait of song length, we conducted a series of two-choice experiments using 18 adult female American goldfinches (Spinus tristis).
The females were given a choice between two male models, one “singing” a shortened version of a typical goldfinch song and the other “singing” a lengthened version of a goldfinch song. To measure within-individual variation, every female was tested twice using identical songs and
14 twice using songs unique to each female. To measure among-individual variation, we compared preference for song length across females for each set of songs (identical and unique). We predicted that female goldfinches will prefer long songs over short songs. Further, we predicted that because birds were tested in isolation, under controlled settings that reduce environmental noise and effects of social context (Chapters 3 and 4), repeatability measures would be high.
METHODS
Study System
The American goldfinch (Spinus tristis) is a small songbird that is abundant and widely distributed across temperate North America (McGraw and Middleton 2009). Typical habitats include weedy fields, orchards, and gardens where they feed in pairs or small groups in spring and during the breeding season (McGraw and Middleton 2009). Additionally, goldfinches are gregarious year-round and are not known to defend food sources nor breeding territories
(McGraw and Middleton 2009). They are mostly socially monogamous (McGraw and
Middleton 2009) and will engage in mate choice copying (Chapter 3). Goldfinches are sexually and seasonally dimorphic. Male goldfinches express multiple conspicuous sexual traits, which vary among individuals and for which females are known to have preferences (e.g., brightness of the bill and nape of the neck, yellowness of the plumage of the epaulets) (Johnson et al. 1993).
These preferences for a variety of male sexual traits makes goldfinches well suited to a study exploring the role of variability of female preferences both within and among individuals.
15 Trapping and Housing
All procedures and facilities for this study were approved by the following: The Ohio
State University Institutional Animal Care and Use Committee (Animal Assurance #A3261-01,
Protocol #2012A00000071), Fish and Wildlife Service Scientific Collecting Permit
(#MB71738A-0), Ohio Division of Wildlife Scientific Collecting Permit (#15-184), Federal Bird
Banding Permit (#22688).
Eighteen wild adult female American goldfinches were trapped and held in captivity for the duration of this study. Trapping locations were Chadwick Arboretum North on The Ohio
State University campus (Columbus, OH, 40°00’39”N 83°01’51”W), Highbanks Metro Park
(Lewis Center, OH, 40°09’01”N 83°02’01”W), and The Dawes Arboretum (Newark, OH,
39°59’43”N 82°25’18”W). Custom-built traps were used to capture birds. The traps were made of 1.27 cm wire mesh (hardware cloth) and measured approximately 38 cm W x 38 cm L x 71 cm H. The traps were designed with several tunnels and larger openings (“windows”) that allowed the birds free access to a feeder that hung inside.
16
Figure 1 Top-down interior view of one of the traps used to catch birds. Visible are the tunnels and at the middle right is one of the “windows.”
Traps were put out at the various locations starting approx. 2–6 weeks in advance of actual trapping and left 24/7. Trapping of birds only took place when a member of the research team was present. Otherwise, the trap functioned essentially as a bird feeder where the birds entered and exited freely. When trapping, the “windows” were covered so that birds attempting to reach the feeders could only enter through the tunnels and, once inside, escape through the
“windows” was prevented. Birds in the trap were then caught by hand.
Male goldfinches were banded and immediately released; female goldfinches were held for study. Banding consisted of marking each bird with a federal metal band on one leg and two plastic coloured bands on the other leg. The 18 females used in this study were trapped during
July 2014. Ten of them were trapped at the Chadwick Arboretum North, seven were trapped at
Highbanks Metro Park, and one was trapped at The Dawes Arboretum. Six of the females were
17 second-year birds (hereafter “younger”) meaning that this was their first breeding season. The remaining twelve females were after-second-year birds (hereafter “older”) meaning that this was their second or later breeding season. Birds were aged using standardized plumage identification techniques (Pyle 1997).
Female goldfinches used in this study were housed indoors in Aronoff Laboratory on The
Ohio State University campus. Temperature (and humidity) was checked at least daily to be between 17° and 29° Celsius (35% average relative humidity). Photoperiod was set to match
July’s peak breeding season sunrise/sunset times. Pairs of birds were kept in commercially purchased standard bird cages. Housing the birds in pairs allowed for social interaction with other females during the period of captivity. In three years of housing birds in this manner, no injuries or serious aggressive interactions between cagemates have been observed (D. Bolen, pers obs.). Standard husbandry procedures were performed daily. A variety of bird seeds
(sunflower, safflower, thistle, millet, etc.) and fresh water were provided ad libitum. A commercially available multi-vitamin supplement for birds and high-calcium grit were also provided. Birds were kept in captivity for approximately 60 days. This length of captivity was necessary to ensure proper separation of trials to avoid problems related to habituation to the trial arena, to adjust photoperiod to match wild conditions at release, and to assist with coordinating of capture and release dates, which often needed to be adjusted due to weather conditions. Birds had ample opportunities to exercise their flight muscles when in the trial arena (as full flight was possible) so that they were healthy and fully capable of flight upon release. At the completion of the study, all females were successfully released at their site of capture.
18 Experimental Design
To measure within and between-individual variation in female preference for short or long songs, 18 adult female American goldfinches were each the subject of four preference trials.
Trials for each female were separated by at least three days. Each trial lasted for 30 minutes.
The trials were conducted in a custom-built arena consisting of three sections: a center and two identical side sections branching off from opposite ends of the center (Fig. 2). Different male taxidermy models were placed in each of the side sections for simultaneous presentation to the observer female. The use of models as “substitutes” for live birds is well established in the literature (e.g., Höglund et al. 1995, Murphy et al. 2014) and helps to control for behavioural differences that might be exhibited among live males.
19
Figure 2 Schematic of the custom-built arena (~ 2.4 m L x 0.9 m W x 0.6 m H) used for preference trials. Floor and walls are solid; top has a wire mesh cover. Dark gray areas represent unused spaces. Brown bars are perches.
Green and pink boxes represent water and food dishes, respectively. Speakers are placed on the floor just outside of the arena; there is a screen “window” in the arena wall just in front of the speakers to allow for sound transmission.
Thin solid lines represent a wire mesh barrier that separates the models from the female. Thick dashed lines represent solid barriers that are raised through the top of the arena via remote pulleys to allow the female access to all areas including perches in front of the models. Models have additional lighting provided by desk lamps containing natural daylight LED bulbs suspended approximately two feet directly above the models at each end of the arena. An opaque curtain surrounded the entire arena. Speaker clipart from
In each trial, we presented the female with a choice between two male taxidermy models.
To give the appearance of “singing,” a goldfinch song recording was played from behind each model (Fig. 2) during each trial (see below for more details on the songs). Four male taxidermy 20 models were used in this study and were randomized across females. All four male models were older birds and in breeding plumage.
To reduce stress from handling and introduction to a new environment, birds were first allowed to acclimate to the arena. During the acclimation period, the female’s movements were restricted to the center section of the arena. Opaque barriers blocked the females’ view of the males. No songs were played during this time. The acclimation period lasted for a minimum of
30 minutes or until the bird was observed exploring, preening, sleeping, bathing, or feeding, whichever came last. If a bird did not meet these criteria within 60 minutes, the trial was terminated. All birds successfully met the criteria for all trials.
Following the acclimation period, to begin each trial, opaque barriers blocking the two side sections were raised and the female was allowed to move freely about the entire arena except for a small area containing the models. If females did not visit both side sections of the arena within 60 minutes of the barriers being raised, the trial was terminated. Three females failed to meet the criteria for one trial each. Data for those trials were not used in any analyses.
After both side sections had been entered by the female, she was observed for 30 minutes.
The four trials consisted of two sets of two trials referred to as ALL1, ALL2, INDIVID1, and INDIVID2 (Fig. 3). By comparing trials ALL1 to ALL2, INDIVID1 to INDIVID2, and comparing across all four trials, we could measure both within-individual and among-individual variation. The presentation order of the trials was randomized among females. Trials ALL1 and
ALL2 presented all of the females with the same two models and the same two playback songs
(one short and one long) such that each female was asked to choose between identical stimuli in two separate trials. To detect either a side bias or a model bias, the arm of the arena playing the short song and the arm playing the long song was switched between trials ALL1 and ALL2; the
21 models were not switched. Which model was presented at which end of the arena was randomized among females. Trials INDIVID1 and INDIVID2 were similar to trials ALL1 and
ALL2 in that each of the females were again presented with the same two models and the same two playback songs (one short and one long) such that each female was asked to choose between identical stimuli in two separate trials. The difference is that the females were tested using playback songs that were only used for that female (and differed from those used in the ALL1 and ALL2 trials). Due to a limited supply of models, each of the females saw the same two models, however, the models were different than the two that they saw for trials ALL1 and
ALL2. Use of the same two models should not pose an issue since any bias based on preference for the models over the songs was being controlled for by switching model-song pairings between trials and also among females.
22
Figure 3 Diagram depicting the 4 trials of each female in the study. Vertical bars within each box represent the separation of the 3 different areas of the arena – the center where the focal female is placed and the 2 ends of each side section of the arena where the models are located. Numbers within the male symbol represent each of the 4 taxidermy male models. Letters beside “song” represent different playback recordings. For ALL1 and ALL2 every female heard the same playback song (i.e., Song A). For INDIVID1 and INDIVID2 females heard a playback song that was unique to each female (i.e., Song B, Song C, etc.) “Short” and “long” indicate the length of the playback songs.
The song being presented in the section of the arena where the female spent the most time was designated as the preferred song (either short or long).
The playback songs were modified using Audacity 2.0.3 (available from https://www.audacityteam.org/) from original recordings acquired from the Borror Laboratory of
Bioacoustics (The Ohio State University, Columbus, OH) of American goldfinch males.
23 Recordings were made between 1953-1986 in various locations around Ohio, with the exception of one recording made in North Carolina. To prepare the playback songs, a procedure similar to that used by Nolan and Hill (2004) was used. A sequence of 10-15 songs in the order they naturally occurred in the recording were identified. Each song was then examined for repetitive song elements. To make short songs, one or more copies of those elements were deleted and, to make long songs, one or more copies of those elements were added. For example, if a particular note was found to repeat eight times in a row, then to make a short song, five of those notes were deleted leaving a sequence of only three repeating notes. Syllable number is one feature of bird song that seems to be important in mate choice (Catchpole 1980). Numerous species have been tested with females exhibiting strong preferences for large song or syllable repertoires (e.g., sedge warbler [Acrocephalus schoenobaenus]: Catchpole 1980, Catchpole et al. 1984; song sparrow [Melospiza melodia]: Searcy 1984). By preparing the playback songs by adding or deleting copies of repeating elements, syllable diversity of the songs remained unchanged.
Similarly, song rate is another important trait that is evaluated by choosy females. Given a choice between males with a high song rate or males with a low song rate, female zebra finches
(Taeniopygia guttata) showed significant preference for males with high song rates (Collins et al.
1994). Similarly, a radio tracking study of 17 female hooded warblers (Wilsonia citrina) found that females that forayed off-territory were more frequently paired with males that sang at a low song rate (Chiver et al. 2008). To hold song rate constant, the intersong intervals were adjusted so that the song rate was equal to 8 songs/minute. The start of one of the songs (either short or long, selected randomly) was offset by 5 s so that during playback, the songs would not be completely overlapping. Additionally, a 60 s silent period was added following the last song in the sequence so that the playback alternated between a period of song and a period of silence.
24 Each playback was sent through a high pass filter at 1,000 Hz and a low pass filter at 20,000 Hz to remove noise, and then normalized to a maximum amplitude of –1.0 dB. The playback was set to loop continuously for the entire trial period. There were a total of 13 short song – long song pairings. One of the 13 was used for trials ALL1 and ALL2, and the remaining 12 were used for trials INDIVID1 and INDIVID2. To avoid any side bias (in addition to the precautions mentioned above), the arm of the arena where playback started first was switched between trials.
Additionally, whether the playback started with a short song or a long song was randomized among females.
To measure time spent in each section of the arena, all trials were recorded using a network camera with live video feed placed directly overhead and centered above the arena.
Recorded trials were reviewed using Windows Media Player 12.0.7601.18741 (Microsoft
Corporation, 2009) and time spent in each section of the arena (center and both side sections) was calculated using JWatcher v1.0 (available from http://www.jwatcher.ucla.edu/).
Statistical Analysis
To examine repeatability of female preference for short or long song, we calculated a song index value as the length of time spent on the side of the arena with the long song divided by the time spent with either song (i.e., not including time spent in the center). Non-significant
Kolmogorov-Smirnoff tests indicated that this variable was normally distributed. Additionally, non-significant Levene’s tests showed that the data met the assumption of equal variance.
Repeatability for the song index and total time spent in the center of the arena was determined by calculating the single measures intraclass correlation coefficients. The single measures intraclass correlation coefficients were calculated for trials ALL1 and ALL2,
25 INDIVID1 and INDIVID2, and across all four trials. To further assess the relationship and strength of correlation of the song index variable, Spearman’s rank correlation coefficients were calculated for trials ALL1 and ALL2 and INDIVID1 and INDIVID2.
We used a generalized estimating equation with a binary probability distribution and logit link function to test our prediction that a female goldfinch will prefer long songs over short songs. The preferred song length (i.e., either short or long) was the dependent variable. The individual female was included as a subject variable and trial was included as a within-subject variable. The model included the main effects of side 1 song length (i.e., short or long) and bird age (i.e., younger or older), and the interaction. Side 1 song length was the length of song that was being played on side 1 of the arena during the trial (Fig. 2) and was included to control for a side bias detected by a binomial test (Z=48.000, N=69, P=0.002). Bird age was included to control for effects of age that have been detected in other studies (Chapter 3). To test for preference, we compared the 95% Wald confidence intervals of the estimated marginal means against a value of 0.5, which would be an equal chance of choosing either short or long song.
The critical value for alpha (α) for all tests was set at 0.05. All analyses were performed using SPSS v25 (IBM Corp., Armonk, NY, USA).
RESULTS
Female goldfinches did not show repeatability of choice for either short or long song
(Table 1). The intraclass correlation coefficient for the song index variable was very small in all three combinations of trials.
Total time spent in the center of the arena was highly repeatable (Table 1). All three combinations of trials had high repeatability values (> 0.7 for INDIVID1 and INDIVID2 and for
26 all four trials). The intraclass correlation coefficient was significantly different from zero for all three combinations of trials (Table 1).
Table 1 Single Measures Intraclass Correlation Coefficients (ICC) to examine repeatability of female choice for short or long song and repeatability of time spent in the center of the arena.
95% CI b Trials ALL1 and ALL2 ICC Lower Upper F df1 df2 P Song Index -0.003a -0.471 0.466 0.994 16 16 0.505 Total Time in Center 0.506 0.049 0.788 3.048 16 16 0.016
Trials INDIVID1 and INDIVID2 Song Index -0.347a -0.711 0.162 0.484 15 15 0.914 Total Time in Center 0.850 0.623 0.945 12.331 15 15 0.000
All 4 Trials Song Index -0.205a -0.272 -0.039 0.318 14 42 0.988 Total Time in Center 0.716 0.503 0.877 11.074 14 42 0.000 a Reported values are negative indicating that model assumptions were violated. b Significant results are in bold.
There was no correlation of the song index values between trials ALL1 and ALL2 (Fig.
4). Similarly, there was no correlation of the song index values between trials INDIVID1 and
INDIVID2 (Fig. 5).
27
Figure 4 Relationship between the song index values in trials ALL1 and ALL2. (Spearman’s=-0.002, N=17,
P=0.993).
28
Figure 5 Relationship between the song index values in trials INDIVID1 and INDIVID2. (Spearman’s=-0.324,
N=16, P=0.222).
Overall, female goldfinches chose short songs over long songs (Table 2). There was a significant effect of side 1 song length (Table 3). Females chose short songs when a short song was being played on side 1 of the arena but chose randomly (i.e., chose long song with a probability of 0.5) when a long song was being played on side 1 (Table 2). There was a significant effect of bird age on female choice for short or long song (Table 3). Younger birds 29 chose short songs over long songs (Table 2). Conversely, older females chose randomly (Table
2).
Table 2 Estimated marginal means and 95% Wald confidence intervals from the main effects of the Generalized Estimating Equation. Means represent the probability of choosing the long song.
95% CIa Model Effect Mean Lower Upper Grand Mean 0.37 0.31 0.45
Side 1 Song Length Short 0.19 0.08 0.39 Long 0.61 0.37 0.80
Bird Age Younger 0.30 0.22 0.41 Older 0.45 0.35 0.55 a Significant results are in bold.
Table 3 Model effects in the Generalized Estimating Equation used to examine the effects of female preference for short or long song. Subject variable is the individual female and within- subject variable is trial.
Model Effect Wald Χ2 Df Pa Side 1 Song Length 3.850 1 0.050 Bird Age 4.075 1 0.044 Side 1 Song Length*Bird Age 0.130 1 0.719 a Significant results are in bold.
30 DISCUSSION
We predicted that within-individual variation in the song index value, which we interpret as a measure of preference, would be low and that among-individual variation in the song index value would be high resulting in repeatability measures that are high. However, we found that female goldfinches show no repeatability of preference for short or long song. The intraclass correlation coefficient for the song index variable was very small in all three combinations of trials indicating that within-individual variation is high relative to among-individual variation.
While many studies have found high and statistically significant repeatability for a variety of mating preference behaviours, others, like our study, have not. High repeatability has been found, for example, in preference for males’ comb colour and size in red jungle fowl (Gallus gallus) (Johnsen and Zuk 1996), number of pulses per trill in the calling songs of field crickets
(Gryllus integer) (Wagner et al. 1995), and for larger males in the poeciliid fish Heterandria
Formosa (Aspbury and Basolo 2002). Conversely, low or no repeatability has been found in preference for male attractiveness in zebra finches (Forstmeier and Birkhead 2004) or call rate and frequency in barking treefrogs (Hyla gratiosa) (Murphy and Gerhardt 2000). In another study examining repeatability of preference for call duration, Gerhardt et al. (2000) found high repeatability in preference for calls of longer duration in the gray tree frog (Hyla versicolor), in contrast to our findings.
The lack of repeatability for the song index found in this study has several possible explanations. A meta-analysis by Bell et al. (2009) found that behaviours measured in the laboratory are less repeatable than behaviours measured in the field. They suggest that greater environmental variation in the field increases the behavioural variation among individuals, increasing repeatability. Bell et al. (2009) also found that mate preference was less repeatable
31 than other types of behaviours (e.g., habitat selection and aggression). It was shown that individuals, mostly females, are not consistent in their mate preferences and that a female’s preference in a mate is subject to change based on context (see also Jennions and Petrie 1997).
Our finding of a lack of repeatability in preference for song length is consistent with this.
We cannot deny that the arena itself may not have been able to accurately capture patterns related to mate choice. We believe this to be an unlikely scenario, however, as subsequent female preference experiments using the same arena did find significant patterns related to the copying of mate choice (Chapter 3) and effects of familiarity among females in altering female preferences (Chapter 4).
Another explanation for the lack of repeatability for the song index could be that females varied in their motivation to mate (Jennions and Petrie 1997). Again, however, we did find significant effects in subsequent studies that took place during the same time of year and used the same arena and general procedures. We also have anecdotal evidence that birds were interested enough in breeding that they were stimulated into laying eggs while in captivity. This happened across years and eggs were laid by more than one bird.
Variation in motivation to mate also could arise if some of the females were shyer than others and did not acclimate well to the arena. Shy individuals tend not to explore as readily as bolder individuals. In rainbow trout (Oncorhynchus mykiss), shy fish were less active and spent less time in an open area than bold fish (Sneddon 2003). Juvenile great tits differed consistently in how they responded to novel objects. Later, when tested in a novel environment, those that had been slower to approach the novel objects were also slower to fully explore the novel environment (Verbeek et al. 1994). In our study, the shyer females may not have engaged with the arena and males as readily as others. This agrees with Carere et al. (2005) who found that
32 slower (shy) great tits (Parus major) took longer to approach a member of the opposite sex than faster (bold) birds. These scenarios might result in what appears to be random choice and lack of repeatability of preference for song.
We found very high repeatability of time spent in the center of the arena. This would be consistent with either variation in motivation to mate or variation in boldness. Variation in these factors among the females could have influenced how much of their time they spent in the center resulting in high among-individual variation relative to within-individual variation. For example, exploratory behaviour of wild great tits (Parus major) is highly repeatable and not related to age or condition (Dingemanse et al. 2002). Boldness is also repeatable under stressful conditions such as high predation risk and exposure to novel objects (Sih et al. 2004,
Dingemanse and Réale 2005). While we do not have the necessary data on boldness-shyness for the females in our study, it would be interesting to see if boldness was correlated with time spent in the center.
Finally, we found a significant side bias which may be preventing us from detecting any patterns related to song preference resulting in the lack of repeatability. The side bias could be related to the experimental procedures used when introducing the birds into the arena. Birds were all placed into the center of the arena from the same side. This may have resulted in birds avoiding the side section of the arena that was adjacent to the side that they were introduced and spending more time in the side section that was farthest away. Subsequent experiments (see
Chapters 3 and 4) did not find a side bias. For those experiments, we altered the introduction of birds by alternating the sides from which they were placed into the arena.
In contrast to our prediction, we found an overall preference for shorter songs.
Preference for longer songs was expected because numerous studies in birds have shown that
33 females prefer males that sing longer songs [white-throated sparrows (Zonotrichia albicollis):
Wasserman and Cigliano 1991; zebra finch: Clayton and Prӧve 1989]. Catchpole et al. (1986) demonstrated that female great reed warblers (Acrocephalus arundinaceus) responded with solicitation displays only to long songs; there was no response at all to short songs. Similarly,
European starling (Sturnus vulgaris) song length is positively associated with female mating preferences (Eens et al. 1991). In blue tits (Parus caeruleus), it was found that extrapair males sang longer songs than the males that they cuckolded (Kempenaers et al. 1997) and, in zebra finches, females whose mates sang longer songs laid on average 0.5 more eggs than when paired with a mate who sang shorter songs (Balzer and Williams 1998). In the more closely related house finch (Carpodacus mexicanus) (Nolan and Hill 2004) and canary (Serinus canaria)
(Pasteau et al. 2009), again, it was found that females preferred long songs over short songs.
Preference for shorter songs has not been previously reported. However, Riebel et al. (2009) did fail to find a directional preference for longer songs in female zebra finches.
Male song length is often an indicator of male quality, therefore, it was surprising that the females in our study preferred shorter songs. Song length is positively correlated with winter dominance in great tits (Parus major). Birds that were dominant in winter survived longer and produced more surviving offspring in their lifetime (Lambrechts and Dhondt 1986). Song length can function as an indicator of fighting ability as in the blue grosbeak (Passerina caerulea) where Lattin and Ritchison (2009) found that longer songs were used during aggressive encounters and that males responded more aggressively to playbacks of longer songs. Song length could be an honest signal for females if singing longer songs imposes a cost on its singers
(Zahavi 1975, Andersson 1994). In hoopoes (Upupa epops), Martín-Vivaldi et al. (1998) found that length of song is positively correlated with body condition. They also found that males
34 reduced mean song length after long singing bouts suggesting that there is some energetic cost associated with singing longer songs. Additionally, song length positively correlates with testosterone levels in wild canaries (Leitner et al. 2001) and European starlings (Riters et al.
2000) and, thus, longer song may be indicative of those males with more resources to invest into the production of elaborate sexual displays. Finally, Martín-Vivaldi et al. (1999) have shown that female hoopoes can directly benefit from choosing males that sing longer songs because those males put greater effort into parental feeding. As a result, females paired with those males produced larger first clutches and laid second clutches more frequently.
The editing of the goldfinch songs to make them shorter or longer may have resulted in the creation of abnormal songs that were outside the range of what females consider normal. We propose three possible explanations: 1) that either both the short and long songs were unnatural sounding, 2) that the short song was more normal than the long song, or 3) that the short song was a supernormal stimulus. Explanation one would likely result in general confusion seen in the lack of repeatability (i.e., high within-individual variation). Alternatively, explanations two and three would explain why we found a trend towards choosing the shorter songs. If the editing of the long song created a song that females no longer recognized as species-specific, they may have defaulted to choosing the short song. However, this disagrees with experiments in which zebra finch songs were created that were up to four standard deviations longer than their normal length and these songs were still preferred by females over shorter songs (Neubauer 1999).
Neubauer (1999) also found a significant preference for songs composed of entirely heterogeneous elements over songs composed of four repeating elements. Our long songs were specifically designed to have multiple repeating notes whereas the short songs had the number of repeating notes reduced. Thus, in comparison, the short songs would have appeared to be more
35 heterogeneous in composition than the long songs even though syllable diversity was held constant. Explanation three suggests that the short song was a supernormal stimulus. Animals often respond more strongly to extreme stimuli that have not been encountered in nature
(Tinbergen and Perdeck 1950, Staddon 1975). Though it seems counterintuitive, the shorter song may have been more extremely altered from normal than the longer songs creating a supernormal stimulus that attracted some of the females.
Repeatability provides a method for measuring variation in preference and provides an upper limit on the estimate of heritability. Because we found no repeatability, heritability of female preference for song length in males in this experiment must also be zero. It is possible that song length is simply not a male trait that female goldfinches use in evaluating potential mates. However, we did find an overall preference for short songs and song length is used in mate choice in the closely related house finch (Nolan and Hill 2004) and canary (Pasteau et al.
2009). We suggest that the lack of repeatability for song length in this study indicates that context strongly influences mating preferences. The female’s social environment might be one such context; in Chapters 3 and 4, we present results of experiments varying social context of choice and find strong influences of the behavior of other females on apparent preferences. If so, sexual selection on male traits may depend heavily on characteristics of the physical and social environment that influence female preference and choice.
36 Chapter 3. EVIDENCE FOR MATE CHOICE COPYING IN A SOCIALLY MONOGAMOUS SPECIES, THE AMERICAN GOLDFINCH (SPINUS TRISTIS)
ABSTRACT
Social factors, such as the mate choice decisions of others, may influence a female’s preference for, or choice of, a particular male as a mate. Mate choice copying occurs when a female is more likely to choose a male as a mate if he has been observed with other females. It is unclear why mate choice copying would be observed in a socially monogamous species when there are direct benefits associated with choosing an unmated male as a mate. Mate choice copying for individual males has not previously been found in a socially monogamous species other than captive zebra finches and even then results have been mixed. We predicted that a female will increase her interest in a less preferred male after observing that male with another female. This prediction was tested with 20 wild-caught female American goldfinches in a series of two-choice preference trials. First, preference between two males, designating one as more preferred and the other as less preferred, was determined. The female was then allowed to see the less preferred male with a female goldfinch, male goldfinch, or female house finch, while the more preferred male remained alone. The female was then tested again to see if her interest in the less preferred male had changed. We found that the difference in the proportion of time spent with the less preferred male increased more after having observed him with another female goldfinch than with a male goldfinch or female house finch. We suggest that copying may occur when choosing extrapair mates but not the social mate. In the context of extrapair mating, using readily available social information, such as the mate choice decisions of other females, may be 37 an effective decision-making strategy. Therefore, despite being a socially monogamous species, goldfinches may use copying when choosing extrapair mates.
INTRODUCTION
Social factors, such as the mate choice decisions of other females, can influence a female’s preference for or choice of a particular male. Mate choice copying, a form of social learning, occurs when a female’s preference for a male increases (or decreases) as a result of observing him being chosen (or rejected) as a mate by another female (Pruett-Jones 1992). This non-genetic transmission of female preferences can act on male ornamentation (Kirkpatrick and
Dugatkin 1994), as well as increase the variance of male mating success (Wade and Pruett-Jones
1990), making it an important evolutionary process. Mate choice copying has been demonstrated in a variety of taxa, including mammals (Galef et al. 2008), fish (Dugatkin 1992,
Dugatkin and Godin 1992, Alonzo 2008 but see Brooks 1996, 1999), and birds (Höglund et al.
1995, Galef and White 1998).
Copying can confer an adaptive advantage to females, especially when differences among males are difficult to distinguish (Wade and Pruett-Jones 1990, Dugatkin and Godin 1993,
Brooks 1996, Vakirtzis 2011) or when there is a cost associated with searching for and evaluating males (Gibson and Höglund 1992, Pruett-Jones 1992). Copying may provide more information about a male than an individual female can gather on her own. Thus, a female constrained by time, for example, may benefit by choosing a mate that has already been evaluated and selected by others, even though she may have reduced benefits in the form of male parental care (Jennions and Petrie 1997). Copying the mating decisions of others will, in
38 general, allow a female to fare better than a female that employs random choice (Wade and
Pruett-Jones 1990).
Alternatively, observing a male with another female may cause avoidance of that male if he is perceived to be already mated or to have mated too frequently (e.g., Harris and Moore
2005, Hamilton et al. 2006). A model by Hamilton et al. (2006) showed that high quality males may attract more unwanted enemy attention (e.g., predators and harassing or sneaker males) due to their increased number of visits by females compared with lower quality males. This may cause a male that is seen with other females to be avoided rather than preferred. Additionally, males that appear to mate frequently may be avoided due to sperm depletion (Warner et al. 1995,
Harris and Moore 2005) or the risk of contracting a sexually transmitted disease (Kokko et al.
2002). Thus, variation in preference for males may result from either a tendency to copy the mate choice of others or a tendency to avoid mate choice copying.
Mate choice copying has been demonstrated in a variety of lekking and promiscuous mating systems (reviewed in Vakirtzis 2011). Vakirtzis and Roberts (2010) state that copying is highly unlikely to evolve in monogamous species. Monogamous females that copy may incur additional costs that would outweigh any benefits of copying. For example, a copying female is likely to suffer from reduced paternal care (Vakirtzis and Roberts 2010). She may also experience costs arising from competition with the male’s current mate (Vakirtzis and Roberts
2010). To date, evidence for mate choice copying in monogamous species has been mixed.
Slagsvold and Viljugrein (1999) failed to find support for mate choice copying in the monogamous pied flycatcher (Ficedula hypoleuca). However, mate choice copying has been found to occur in the socially monogamous zebra finch (Taeniopygia guttata) (Swaddle et al.
2005; Drullion and Dubois 2008; Kniel et al. 2015a, 2015b but see Doucet et al. 2004).
39 Additional studies are needed to broaden the taxonomy base to further find support for or against this evolutionarily important alternative mate choice strategy.
The American goldfinch (Spinus tristis), like the zebra finch, is a socially monogamous species known to be gregarious year-round (McGraw and Middleton 2009) but varies from the zebra finches previously studied in several important ways. First, wild zebra finches live in semiarid and arid regions of Australia. Breeding is unpredictable and opportunistic often following a sizeable rainfall event (Zann 1996). On the other hand, goldfinches are native to temperate North America and have a predictable, albeit short, breeding season (McGraw and
Middleton 2009). Second, the zebra finches previously studied were part of captive colonies
(Doucet et al. 2004; Swaddle et al. 2005; Drullion and Dubois 2008; Kniel et al. 2015a, 2015b) and the onset of breeding was artificially stimulated (Doucet et al. 2004). The goldfinches in the study described here were wild-caught during their normal breeding season.
Several aspects of goldfinch breeding biology suggest that copying may be a successful alternative strategy for mate choice for females of this species. Goldfinch pair bonds are presumably formed in winter flocks while nesting does not take place until mid to late summer
(McGraw and Middleton 2009). This gives females plenty of time to observe the mate choices of others. Social information may also be used to evaluate potential extrapair mates (Doucet et al. 2004, Dubois 2007). Extrapair matings are common in monogamous systems (Griffith et al.
2002) and occurs in goldfinches. Extrapair paternity of 14.3% of 70 offspring in 27% of 15 broods has been found in goldfinches (Gissing et al. 1998). Goldfinch nests are frequently clumped in “loose colonies” (McGraw and Middleton 2009) giving females opportunities to both observe and engage in extrapair matings. Finally, if a first nesting is successful, female goldfinches are known to abandon the first brood to their social mate in order to permit a second
40 nesting with a new mate (McGraw and Middleton 2009). If, at the time of a second nesting, most males are either still paired or caring for a first brood, then the father of a second brood may likely be an extrapair mate. Copying may be a strategic tactic for ensuring a high quality father for a second brood. Alternatively, goldfinches are mostly socially monogamous, so that females may avoid mating with already mated males. Additionally, because male goldfinches provide parental care to chicks and feed the female while she is incubating (McGraw and
Middleton 2009), female-female competition for males that can invest more time in parental behaviours may cause females to prefer unmated partners.
In this study, we tested female goldfinches for mate choice copying of individual males by using a series of two-choice preference trials. After an initial preference test to determine the more preferred and less preferred males, the female observed the less preferred male in the company of either a female goldfinch, a male goldfinch, or a female house finch. After these observations, the female was then tested again to see if the time she spent near the less preferred male had changed. For mate choice copying, we predicted that a female goldfinch would increase time spent with a less preferred male after observing that male in the company of another female goldfinch. If females avoid previously mated males, we predicted that a female goldfinch would decrease time spent with a less preferred male after observing him in the company of another female goldfinch.
METHODS
Trapping and Housing
All procedures and facilities for this study were approved by the following: The Ohio
State University Institutional Animal Care and Use Committee (Animal Assurance #A3261-01,
41 Protocol #2012A00000071), Fish and Wildlife Service Scientific Collecting Permit
(#MB71738A-0), Ohio Division of Wildlife Scientific Collecting Permit (#16-147), Federal Bird
Banding Permit (#22688), Ohio Division of Wildlife Banding Permit (#18-105).
Twenty wild adult female American goldfinches were trapped and held in captivity for the duration of this study. Trapping locations were Chadwick Arboretum North and Waterman
Agriculture and Natural Resources Laboratory Complex on The Ohio State University campus
(Columbus, OH, 40°00’39”N 83°01’51”W), Highbanks Metro Park (Lewis Center, OH,
40°09’01”N 83°02’01”W), and The Dawes Arboretum (Newark, OH, 39°59’43”N
82°25’18”W). Custom-built traps were used to capture birds. The traps were made of 1.27 cm wire mesh (hardware cloth) and measured approximately 38 cm W x 38 cm L x 71 cm H. The traps were designed with several tunnels and larger openings (“windows”) that allowed the birds free access to a feeder that hung inside.
Traps were put out at the various locations from approx. 2–6 weeks in advance of actual trapping and left 24/7. Trapping of birds only took place when a member of the research team was present. Otherwise, the trap functioned essentially as a bird feeder where the birds entered and exited freely. When trapping, the “windows” were covered so that birds attempting to reach the feeders could only enter through the tunnels and, once inside, escape through the “windows” was prevented. Birds in the trap were then caught by hand.
Male goldfinches were banded and immediately released; female goldfinches were held for study. Banding consisted of marking each bird with a federal metal band on one leg and two plastic coloured bands on the other leg. The 20 females used in this study were trapped during
June thru early July 2015. Ten of them were trapped at Highbanks Metro Park, five were trapped at The Dawes Arboretum, three were trapped at the Chadwick Arboretum North, and two
42 were trapped at the Waterman Agriculture and Natural Resources Laboratory Complex. Nine of the females were second-year birds (hereafter “younger”) meaning that this was their first breeding season. The remaining eleven females were after-second-year birds (hereafter “older”) meaning that this was their second or later breeding season. Birds were aged using standardized plumage identification techniques (Pyle 1997).
Female goldfinches used in this study were housed indoors in Aronoff Laboratory on The
Ohio State University campus. Temperature (and humidity) was checked at least daily to be between 17° and 29° Celsius (35% average relative humidity). Photoperiod was set to match
July’s peak breeding season sunrise/sunset times. Pairs of birds were kept in standard bird cages.
Housing the birds in pairs allowed for social interaction with other females during the period of captivity. In four years of housing birds in this manner, no injuries or serious aggressive interactions between cagemates have been observed. Acoustic and visual interactions were also possible with birds in neighboring cages. Standard husbandry procedures were performed daily.
A variety of bird seeds (sunflower, safflower, thistle, millet, etc.) and fresh water were provided ad libitum. A commercially available multi-vitamin supplement for birds and high-calcium grit were also provided. Birds were kept in captivity for no more than 60 days. This length of captivity was necessary to ensure proper separation of trials to avoid problems related to habituation to the trial arena, to adjust photoperiod to match wild conditions at release, and to assist with coordinating of capture and release dates, which often needed to be adjusted due to weather conditions. Birds had ample opportunities to exercise their flight muscles when in the trial arena (as full flight was possible) so that they were healthy and fully capable of flight upon release. At the completion of the study, all 20 females were successfully released at their site of capture.
43 Experimental Design
After a minimum of seven days in housing, each female was the subject of a series of three preference trials. With two exceptions, trials for each female were separated by at least eleven days. Trials for the two exceptions are detailed below and took place after two (for female orange/medium blue) and three days (for female black/yellow). The trials were conducted in a custom-built arena in which the female was placed in the center and two competing stimuli were presented simultaneously at opposite ends of the arena (Fig.2). Birds were first allowed to acclimate to the arena. During this time, the female’s movements were restricted to the center section of the arena. The acclimation period lasted for 30 minutes or until the bird was observed exploring, preening, sleeping, bathing, or feeding, whichever came last. If a bird did not meet these criteria within 60 minutes, the trial was terminated. All birds successfully met the criteria for all trials.
Each trial consisted of three, 30-minute phases: pre-test, observation, and post-test (Fig.
6). At the start of each phase, opaque barriers blocking the competing stimuli were raised and the female was allowed to move freely about the entire arena except for a small area containing the stimuli. If females did not visit both ends (arms) of the arena within one hour of the barriers being raised, the trial was terminated. Only two trials were not initially successful: One due to an equipment issue (female black/yellow) and a second caused by researcher error (female orange/medium blue). Therefore, a repeat of the affected trial for each of the birds was added to the end of the trial schedule. In all trials, each 30-minute phase began as soon as both arms had been entered by the female. All trials were recorded using a network camera with live video feed placed directly overhead and centered above the arena. Recorded trials were reviewed using
Windows Media Player 12.0.7601.18741 (Microsoft Corporation, 2009) and time spent in each
44 section of the arena (center and both arms) was calculated for the observation and post-test phases using JWatcher v1.0 (available from http://www.jwatcher.ucla.edu/).
Figure 6 Diagram depicting the relationship between trial, phase, and treatment. Treatments took place during the observation phase of each trial. During the pre-test and post-test phases, both the more preferred and less preferred males are alone. Vertical bars within each box represent the separation of the 3 different areas of the arena – the center where the focal female is placed and the 2 ends of each arm of the arena where the models are located.
GF=goldfinch, HF=house finch. ♂+ = the more preferred male, ♂- = the less preferred male.
In the pre-test, we presented the female with a choice between two male taxidermy models (see Supplemental Material for more details on the models). To give the appearance of
“singing,” a goldfinch song recording was played from behind each model (Fig. 2) during each phase of each trial (see Supplemental Material for more details on the songs). The more preferred and less preferred males were determined by calculating the amount of time the female 45 spent in each arm of the arena. The pre-test phase was viewed live and time spent in each section of the arena was measured in real time using JWatcher. The male in the arm of the arena where the female spent the most time during the 30-minute pre-test was designated as the more preferred male and the other male was designated as the less preferred male. These designations did not change in subsequent phases (i.e., the less preferred male from the pre-test is referred to as the less preferred male throughout, even if the female’s preferences changed). Following the pre-test, the barriers were lowered and the female was confined to the center of the arena while one of three observation treatments, randomized among females, followed (Fig. 6). For the observation treatments, we placed next to the less preferred male a taxidermy model of a female goldfinch or one of two controls: a male goldfinch or a female house finch (Carpodacus mexicanus) (see Supplemental Material for more details on the models). In all three treatments, the more preferred male remained alone. The male goldfinch treatment controlled for whether the presence of another female goldfinch, or just another goldfinch, was needed to influence a female’s preference for the less preferred male; also, whether a female simply prefers to be near greater numbers of birds. The female house finch treatment controlled for whether a preference to be near greater numbers of birds applies only to groupings of goldfinches, or if females prefer to be social regardless of species group composition. Song recordings used during the observation phase included one additional element from the pre-test and post-test recordings.
For the male goldfinch treatment, one additional copy of the male song already being played was added to give the appearance of a third male singing. For the female goldfinch and female house finch treatments, recordings of female courtship calls were overlaid on the playbacks of the singing males (see Supplemental Material). Once the treatment bird for the observation phase was in place, the barriers were raised for 30 minutes and the female was then able to observe
46 both the more preferred male by himself and the less preferred male now in the company of another bird. Following the observation phase, the barriers were lowered and the female was again restricted to the arena’s center. The female goldfinch, second male goldfinch, or house finch model was removed so that both of the original males were now alone as in the pre-test.
For the post-test, just as in the pre-test, the barriers were raised and the amount of time the female spent in each section of the arena during a 30-minute period was measured.
Statistical Analysis
The critical value for alpha (α) for all tests (except as noted) was set at 0.05. All analyses were performed using SPSS v25 (IBM Corp., Armonk, NY, USA).
In most analyses, the dependent variable was the difference in the proportion of time spent with the less preferred male from the post-test to the pre-test phase. The proportion of time spent with the less preferred male was calculated as the time spent with the less preferred male divided by the time spent with either male (i.e., not including time spent in the center). This value was calculated for all of the three phases of a trial. Visual inspection of Q-Q plots along with non-significant Kolmogorov-Smirnoff tests indicated that this variable was normally distributed. Additionally, non-significant Levene’s tests showed that the data met the assumption of equal variance.
We used a generalized estimating equation with a normal probability distribution and identity link function to test our prediction that a female goldfinch will increase the proportion of time spent with a less preferred male after observing that male in the company of another female goldfinch. The difference in the proportion of time spent with the less preferred male over time spent with either male from the pre-test to the post-test phase was the dependent variable. The
47 individual female was included as a subject variable and treatment was included as a within- subject variable. The model included the main effects of treatment, bird age, and trial order and all two-way interactions. The three-way interaction was not included in the model due to problems with estimating standard error which could not be explained from the data; results of models that included the three-way interaction did not differ qualitatively from those reported here (unpublished data). For post hoc analyses, significance of the pairwise contrasts was assessed using Fisher’s Least Significant Differences, adjusted using a Bonferroni correction for multiple comparisons. All tests were two-tailed.
RESULTS
Several analyses were completed to make sure that the observed results were due to the experimental procedure and not caused by any inherent biases related to the arena, the song recordings, or any of the taxidermy models. A binomial test showed no side bias related to the arena with females in 55% of the trials preferring the male model on one side and 45% preferring the male model on the other side (Z=27.000, N=60, P=0.519). We checked for unresponsiveness
(defined as the time it took for the bird to visit both arms of the arena to start the pre-test phase) that may have been due to the song recordings with a generalized estimating equation and found
2 no significant effect of song (Wald Χ 2=1.258, P=0.533). For the four male models, we looked at both whether any of the models was chosen significantly more often as the more preferred male or, similarly, whether any of the models was designated more often as the less preferred male. The results of both Chi-square tests were that no one model was significantly preferred
2 2 (Χ 3=1.733, P=0.630), or not preferred (Χ 3=1.333, P=0.721), over any other model.
48 Females increased time spent near the less preferred male more when he was paired with a female goldfinch than paired with a male goldfinch or female house finch. There was a significant effect of treatment on the difference in the proportion of time spent near the less preferred male from the pre-test to the post-test phase (Table 4), with a larger increase after he
Table 4 Generalized Estimating Equation to examine the effects of treatment, bird age, and trial order on the difference in the proportion of time spent with the less preferred male over time spent with either male from the pre-test phase to the post-test phase. Subject variable is the individual female and within-subject variable is the treatment.
Model Effect Wald Χ2 Df Sig.a Treatment 15.226 2 0.000 Bird Age 0.839 1 0.360 Trial Order 1.099 2 0.577 Treatment*Bird Age 16.065 2 0.000 Treatment*Trial Order 38.246 4 0.000 Bird Age*Trial Order 13.557 2 0.001 a Significant results are in bold.
was observed paired with a female goldfinch than when he was observed paired with a male goldfinch (P<0.000) or a female house finch (P=0.014) (Fig. 7). There was not a significant difference between the male goldfinch treatment and the female house finch treatment
(P=0.751).
49
Figure 7 The difference in the proportion of time spent with the less preferred male over time spent with either male from the pre-test phase to the post-test phase based on the treatment. Treatments are the bird (female goldfinch, male goldfinch, female house finch) observed with the less preferred male during the observation phase.
N=20 for each treatment. Columns represent the mean. Error bars represent 95% CI. NS=not significant,
*=significant at P<0.05, **=significant at P<0.000 (Generalized Estimating Equation, main effect=treatment, Wald
2 Χ 2=15.226, P<0.000).
Older females were selectively influenced by the presence of another female goldfinch whereas younger birds increased time spent with the less preferred male equally across all treatments. We found a significant effect of the interaction between treatment and the age of the
2 focal female (Wald Χ 2=16.065, P<0.000) (Table 4). Within younger birds there are no significant differences among treatments (Fig. 8). Within older birds, the female goldfinch treatment is significantly different from both the male goldfinch treatment (P<0.000) and the
50 female house finch treatment (P<0.000). Older females increased the proportion of time spent with the less preferred male more when the treatment bird was another female goldfinch than when either a male goldfinch or a female house finch. The male goldfinch and female house finch treatments were not significantly different from one another (P=0.357). Within treatments, the increased time spent with the less preferred male from the pre-test to the post-test is not significantly different after Bonferroni correction between younger and older females (female goldfinch: P=0.046; male goldfinch: P=0.027; female house finch: P=0.212).
51
Figure 8 The difference in the proportion of time spent with the less preferred male over time spent with either male from the pre-test phase to the post-test phase based on the treatment and age of the focal female. Treatments are the bird (female goldfinch, male goldfinch, female house finch) observed with the less preferred male during the observation phase. N=20 for each treatment. “Younger” females are those in their first breeding season (N=9);
“older” females are those in their second or later breeding season (N=11). Columns represent the mean. Error bars represent 95% CI. **=significant at P<0.000 (Generalized Estimating Equation, interaction=treatment*bird age,
2 Wald Χ 2=16.065, P<0.000).
Females increased the proportion of time spent with the less preferred male more during the second and third round of trials, but not during the first round, after observing him paired with another female goldfinch rather than a male goldfinch or female house finch. We found a
2 significant effect of the interaction between treatment and order of the trials (Wald Χ 4=38.246,
P<0.000) (Table 4). For round one of trials, which was the birds’ first experience in the arena,
52 there was not a significant effect of treatment on the difference in the proportion of time spent with the less preferred male from the pre-test to the post-test phase (Fig. 9). However, in the
Figure 9 The difference in the proportion of time spent with the less preferred male over time spent with either male from the pre-test phase to the post-test phase based on the treatment and order of trials. Treatments are the bird
(female goldfinch, male goldfinch, female house finch) observed with the less preferred male during the observation phase. N=20 for each treatment. Presentation of the treatments was randomized among females across trials.
Columns represent the mean. Error bars represent 95% CI. *=significant at P<0.05 (Generalized Estimating
2 Equation, interaction=treatment*trial order, Wald Χ 4=38.246, P<0.000).
second and third round of trials, there was a significant effect of treatment, with birds in the female goldfinch treatment increasing time spent with the less preferred male more than those in
53 the male goldfinch (trial 2: P=0.004; trial 3: P=0.004) and female house finch treatments (trial 2:
P=0.001; trial 3: P=0.005). The male goldfinch and female house finch treatments are not significantly different from each other (trial 2: P=0.568; trial 3: P=0.277). In all cases, within treatments, the difference in the proportion of time spent with the less preferred male from the pre-test to the post-test did not differ significantly between round two and round three of trials
(female goldfinch: P=0.734; male goldfinch: P=0.551; female house finch: P=0.949).
DISCUSSION
We hypothesized that a female’s mate choice preferences are influenced by the mate choice decisions of other females and predicted that, if mate choice copying occurs, time spent with the less preferred male would increase between the pre-test and post-test phases for the female goldfinch treatment more so than for the controls (i.e., male goldfinch or female house finch treatments). Conversely, if avoidance of previously mated males occurs, we predicted that time spent with the less preferred male would decrease between the pre-test and post-test phases for the female goldfinch treatment more so than for the controls. Results support the hypothesis of mate choice copying in female goldfinches. The magnitude of the change in time spent near the less preferred male was significantly greater after that male was observed paired with a female goldfinch than if paired with a male goldfinch or female house finch.
We found evidence for copying of preferences for individual males in female goldfinches. Swaddle et al. (2005) also found evidence that social information can shift female preferences for particular males in socially monogamous zebra finches. However, in that study, females required two weeks of social observation before such a shift occurred, and studies using a shorter observation period did not find an effect of copying (Slagsvold and Viljugrein 1999,
54 Doucet et al. 2004). We saw a shift in interest in the less preferred male after just 30 minutes of observation. Kniel et al. (2015a, 2015b) also found evidence for copying. However, they were testing for shifts in preferences for novel phenotypes rather than preferences for individual males. Likewise, Drullion and Dubois (2008) used different males in their initial and final preference experiments so that evidence for copying was based on phenotype preferences and not preferences for individual males. Our findings are contrary to Slagsvold and Viljugrein
(1999) and Doucet et al. (2004), who did not find support for copying of individual males. By using taxidermy models rather than live birds (see Supplemental Material), we controlled for any variation in both male or demonstrator female behaviour that may have influenced the results of these and other studies (Swaddle et al. 2005, Kniel et al. 2015a and 2015b, and Drullion and
Dubois 2008 who used videos of live birds). The use of models as “substitutes” for live birds is well established in the literature (e.g., Höglund et al. 1995, Murphy et al. 2014).
Why would a socially monogamous female benefit from copying the mate choices of another female given that there are direct benefits associated with choosing an unmated male as a mate? We suggest that copying may occur when choosing extrapair mates but not the social mate. Vakirtzis and Roberts (2010) state that males of higher genetic quality will have more extrapair copulations but suggest that potentially copying females will probably be unaware of these typically covert matings. We offer that copying females may be more alert to extrapair copulations than suggested, as females of socially monogamous species are known to engage in extraterritorial forays for the purpose of seeking extrapair copulations (e.g., northern cardinals
[Humbird and Neudorf 2008], common yellowthroat [Pedersen et al. 2006], superb fairy-wrens
[Double and Cockburn 2000]) and can observe extrapair copulations involving conspecific females at such times. It is also possible that extraterritorial forays are made partly for the
55 purpose of evaluating future extrapair mates and may include observing which individuals are engaging in extrapair copulations. Additionally, some species have specialized extrapair copulation displays (Dickinson et al. 2000) and females that call to advertise for potential extrapair mates (Neudorf et al. 2008) so that any extrapair interactions would not necessarily be covert.
As an alternative, we had predicted that because goldfinches are mostly socially monogamous, females might avoid mating with already mated males. Because male goldfinches provide parental care to chicks and feed the female while she is incubating (McGraw and
Middleton 2009), female-female competition for males that can invest more time in parental behaviours may cause females to prefer unmated partners. Evidence for the reverse of mate choice copying has been found by Brooks (1999). He found that feral guppies not only showed no tendency towards copying the mate choice of other females, but that they actually avoided the side of the tank on which they had previously observed a female being courted. Other explanations for avoiding males seen with other females include unwanted enemy attention from predators and harassing or sneaker males (Hamilton et al. 2006) and sperm depletion (Warner et al. 1995, Harris and Moore 2005). However, our result that time spent with the less preferred male increased after observing him with another female goldfinch do not support any of these explanations for females seeking social mates. If females use copying to find extrapair mates, then this would explain why we found a lack of avoidance of apparently chosen males.
We found a significant effect of the interaction between treatment and the age of the focal female. Previous studies indicate that female preferences can vary with age (e.g., Coleman et al.
2004) and a model by Kirkpatrick and Dugatkin (1994) investigated mate choice copying in which younger females are influenced by the choices of older females. Similarly, Dugatkin and
56 Godin (1993) showed that younger female guppies were more likely to copy than older females, and Laland (2004) suggests that a prudent social learning strategy is to copy older individuals.
In these instances, it may be that younger females have poorer discrimination abilities and thus rely more on social information from other females about potential mates (Dugatkin and Godin
1993, Kirkpatrick and Dugatkin 1994, Jennions and Petrie 1997). However, we found that older birds spent more time with the less preferred male only after the female goldfinch treatment whereas younger birds increased time spent with the less preferred male after all the treatments.
Older males are more likely to sire extrapair young and pursue extrapair copulations (e.g.,
Dickinson 2001, Bitton et al. 2007, Schmoll et al. 2007, Reitsma et al. 2018), and this may also be true for older females. Rӓtti et al. (2001) found that, in their study of pied flycatchers, all cases of extrapair fertilizations involved older females mated with younger males. Similarly,
Bouwman and Komdeur (2005) found that older females tended to have higher levels of extrapair paternity in their broods, especially when mated with younger males. If our females were seeking extrapair mates rather than social mates as we suggested, the age of the female may influence how and when copying factors into this process, which future work may elucidate.
We found that female goldfinches increased time spent with a less preferred male after observing him paired with another bird in 85% of the trials, however, females did not always switch their preference from the more preferred male (as determined during the pre-test) to the less preferred male after having observed him with another bird. We cannot predict how the results of such a choice test as we have conducted here might translate to actual reproductive decisions. However, the shift in time spent with the less preferred male as a consequence of observing that male with another female is a more meaningful measure of the influence of social information than reporting a shift in choice. Simple dichotomous scoring of two-choice tests
57 lacks the resolution necessary to demonstrate variation in the strength of preferences without repeated testing of each set of stimuli (Wagner 1998).
We did not find evidence that a female is attracted merely to the presence of two individuals or two goldfinches over the presence of just one individual (e.g., male alone).
Goldfinches are social. Therefore, their preference for a location might increase as the result of observing greater numbers of other birds at that location. However, our results indicate that the females’ preferences for the less preferred male were selectively influenced only by the presence of another female goldfinch, at least for older birds. Similarly, Dugatkin (1992) tested to see if female guppies were simply attracted to greater numbers of fish but found no tendency for the focal female to prefer the area that had recently had two fish to the area that had contained only one fish. White and Galef (1999) found that only the presence of another female Japanese quail
(Coturnix coturnix japonica), not another male, increased the affiliation time of the observing female towards a previously non-preferred male.
A potential issue in repeated measures analyses, including studies of change of attractiveness, is regression toward the mean where an extreme value will tend to be followed by a value closer to the mean (Kelly and Price 2005). Regression toward the mean would not predict our observed differences among the treatments with the female goldfinch treatment being significantly different from the male goldfinch and female house finch treatments. If regression toward the mean had occurred, we would not have found a significant effect of treatment.
Understanding the factors that can influence decisions as important to an individual’s fitness as mate choice can inform studies of sexual selection and evolution. Variability in female preferences can affect the intensity and direction of selection on male sexual traits (Gibson and
Höglund 1992), as well as explain variation in male reproductive success (e.g., Wade and Pruett-
58 Jones 1990, Andersson 1994, but see Kirkpatrick and Dugatkin 1994). The potentially vital role that a female’s social life may play in the variability of preferences and, ultimately, her decision- making should not be overlooked (Jennions and Petrie 1997, Westneat et al. 2000). We see a need for studies that follow the copying process through to actual mate choice and reproduction.
Copying can be a powerful selective force, but we need to know more about the actual fitness consequences of copying to both males and females to understand its impact on the evolution of mating systems, mate choice, and traits under intersexual selection.
SUPPLEMENTAL MATERIAL
Models
Four male taxidermy models were used in this study and were randomized across females. Females saw each of the males twice, but the same pairings of males was avoided.
Over the three trials, each female saw three of the four models but the pairings of males differed for each trial. To avoid any effect of familiarity, the male goldfinch model presented as the treatment bird during the male goldfinch observation was unfamiliar to each female (i.e., was never presented to the female during one of the other trials). All four male models were older birds. There were two female goldfinch taxidermy models (both older birds). During the female goldfinch trials, half of the females saw one model, half saw the other. Similarly, there were two female house finch taxidermy models (both younger birds). During trials, half of the females saw one, half saw the other.
59 Songs
One of three goldfinch song recordings were played during each trial to give the appearance that the male models were “singing”. The recordings, acquired from the Macaulay
Library at the Cornell Lab of Ornithology, were made in Maryland (May 1998), Tennessee (June
1994), and California (April 1991). A section of continuous male goldfinch song (average of 5 minutes 30 seconds) was taken from each recording. Each section was unaltered, with the exception of being put through a high pass filter at 1,000 Hz to remove low frequency noise.
Each section of song was repeated twice with 2-4 minutes of silence added after each section so that the playback alternated between periods of song and periods of silence. Using Audacity
2.0.3 (computer software audio editor, available from http://audacity.sourceforge.net/), the resulting playbacks (average of 17 minutes) were set to loop continuously during each phase of each trial.
The pairing of playback recordings with trials was randomized among females, and each female heard each recording only once. To control for differences in preference between two males based on song, both males being presented to the female during each of the phases of a trial were singing the same song. However, to prevent it from sounding like they were singing in unison, the beginning of playback for the males was offset by 30 seconds so that for the duration of the playback loop there were times when each male was singing by himself and times when their singing overlapped. Additionally, playbacks were constructed so that males would alternate between which started singing first after each period of silence for as long as the playback looped. This controlled for any preference biases that may be directed toward the male that was heard singing first.
60 Playbacks used during the observation phase of each trial included one additional element from the structure described above. For the male goldfinch treatment, to give the appearance of three males singing, one more copy of the same section of song specific to each recording was added to the playback. Again, so as not to bias the female, all three males were singing the same song. For the female goldfinch and female house finch treatments, recordings of female courtship calls were overlaid on the playbacks of the singing males. The female vocalizations along with the male singing were intended to both standardize and simulate female interest in the less preferred male. The recording for the female goldfinch treatment, acquired from the
Macaulay Library, was made in New York (August 1952). An unaltered section (approx. 34 seconds long) consisting of courtship calls was used for the playback. The recording for the female house finch treatment (approx. 34 seconds long, unaltered) was also acquired from the
Macaulay Library and was made in Baja California (October 1997). For both of the female treatments, the sections with the female calls were repeated 10 times per playback loop.
61 Chapter 4. FAMILIARITY AMONG FEMALES INCREASES MATE CHOICE COPYING IN THE AMERICAN GOLDFINCH (SPINUS TRISTIS)
ABSTRACT
The social environment can influence female choice for mates. A female may be more likely to choose a male that has been observed with other females (mate choice copying).
Copying can be costly, however, if a female obtains inaccurate information from another female.
Because familiar females are likely to share similar environments and experiences, a female may benefit more from copying them rather than unfamiliar females. We predicted that females would spend more time with a previously less preferred male after observing him with a familiar rather than an unfamiliar female. We presented 24 wild-caught female American goldfinches with a choice between two potential mates in a series of two-choice preference trials. After determining which of the two males is more preferred by the observer female, she observed the initially less preferred male with a demonstrator female that was either familiar or unfamiliar to the observing female. The observer female was then tested again to measure the change in time spent with the less preferred male. We found that time spent with the less preferred male increased more after he was observed with a familiar female rather than an unfamiliar female.
While effects of familiarity have been found in other contexts, we show here that familiarity influences copying the apparent mate choices of others. This suggests an important potential role of female-female social relationships on male reproductive success and the evolution of male characteristics.
62 INTRODUCTION
Social learning occurs when animals acquire information about their environment by observing the behaviours of others (Coussi-Korbel and Fragaszy 1995). Behaviours learned socially include when and where to forage for food (Laland and Williams 1997, Galef and
Giraldeau 2001, Reader et al. 2003) or use of tools (Inoue-Nakamura and Matsuzawa 1997, Tan et al. 2018). Social learning can also influence decisions regarding potential mates (Jennions and
Petrie 1997). Mate choice copying occurs when a male is more likely to be chosen simply because he was observed with other females (Chapter 3; Dugatkin 1992; Dugatkin and Godin
1992, 1993; Gibson and Höglund 1992, Pruett-Jones 1992, Galef and White 1998). Mate assessment in this social context allows a female to use information gathered from other females about potential mates, in addition to the information gathered on her own. This can have consequences for intersexual selection, for example, cultural transmission of preferences can result in selection on male ornamentation (Kirkpatrick and Dugatkin 1994). Therefore, decisions about whether, when, and from whom to copy could influence the transmission of social information and affect the evolution of both female preferences and male characteristics.
Copying the choices or behaviours of others is often beneficial as it allows the observer
(or copier) to avoid the costs associated with asocial learning (Laland 2004). For example, juvenile guppies trained with demonstrators from a high predation area significantly improved their antipredator behaviours over those trained with demonstrators from a low predation area
(Kelley et al. 2003). Similarly, observers paired with demonstrators trained to one of two escape routes swam more quickly and more often through the escape route to which the demonstrators had been trained (Reader et al. 2003). Copying may also be beneficial when an animal is
63 uncertain because it possesses no relevant prior knowledge about a novel environment, or when established behaviors are unproductive (Laland 2004).
However, copying can also incur risks of gaining inaccurate or unreliable information
(Laland 2004). For example, social groups of guppies (Poecilia reticulata) were trained to take one of two routes, either short or long, to food. Untrained guppies continued to take the long energetically costly route even after all the trained guppies had been replaced (Laland and
Williams 1998). This demonstrates that copying can transmit maladaptive information. Perhaps one of the greatest risks of copying is that the copier does not learn to read and respond to cues about its environment appropriately. Beauchamp and Kacelnik (1991) trained zebra finches to recognize that a red light signaled that food was available (knowledgeable birds). They found that naïve birds paired with a knowledgeable partner learned more slowly about the signal than those birds paired with a non-knowledgeable partner. They reasoned that the naïve birds learned to cue off the knowledgeable partner rather than the signal itself. Information cascades – when an observer only has information about the behavioural decisions of others and not the actual cues that those decisions were based upon – can lead to the repeated transmission of unreliable information (Giraldeau et al. 2002). This might cause an observer to reject a high quality resource or to accept one of poor quality. Mate choice copying may lead to some risk of an informational cascade (Gibson and Hӧglund 1992). If every member of the population acquired all of their information strictly through copying, new and reliable information about the environment acquired by asocial learners would not be contributed, so that the benefits of copying are negatively frequency dependent (Laland 2004). Because of the costs and risks associated with social learning, individuals are expected to be selective about when they acquire and use social information and about which individuals they copy (Laland 2004).
64 Coussi-Korbel and Fragaszy (1995) suggest that the characteristics of both the demonstrator and observer function to influence acquisition and use of social information
(“directed social learning”). For example, adult laying hens (Gallus gallus domesticus) learned a keypecking task for a food reward quicker from socially dominant demonstrators than from socially subordinate demonstrators (Nicol and Pope 1994). Similarly, young guppies were found to be more likely to copy the mate choice of older, more experienced females (Dugatkin and
Godin 1993), and female sailfin mollies (Poecilia latipinna) significantly increased time spent with a previously non-preferred male after observing him with a high quality female (i.e., a conspecific female) and decreased time spent after observing him with a low quality female (i.e., a heterospecific female) (Hill and Ryan 2006).
Familiarity among the demonstrator-observer pair is another characteristic that may influence the likelihood of social learning. Familiar individuals are more likely to spend more time in each other’s presence and to experience similar environments than are unfamiliar individuals (Laland 2004). Observers may pay more attention to familiar individuals due to proximity and shared experiences. For example, Lachlan et al. (1998) found that female guppies
(Poecilia reticulata) preferred to shoal with familiar individuals rather than unfamiliar individuals. They suggest that guppies may be more likely to learn from familiar rather than unfamiliar conspecifics. Familiar females, due to experiencing similar environments, may have similar socially-acquired mate preferences. The roles that proximity and shared experiences play in mate choice copying are not known.
In addition, familiarity can reduce costs associated with aggressive encounters between observers and demonstrators. Females can compete with each other for a variety of reasons, including resident female aggression toward intruders (Slagsvold and Lifjeld 1994). Previous
65 studies on familiarity among females (Ferkin 1988, Zhang et al. 2001) and the “dear enemy” hypothesis both suggest that, most of the time, aggressive encounters are reduced when the parties involved have some level of familiarity with one another (Bradbury and Vehrencamp
2011). If mate choice copying occurs in the context of extrapair copulations (Chapter 3), familiarity may better allow females to enter and observe occupied territories. Therefore, we suggest that by lessening the intensity or frequency of aggressive encounters occurring due to female-female competition, familiarity can facilitate acquisition of social information about potential mates.
While several studies have examined the effects of familiarity between females and males on mate choice (Kelley et al. 1999, Zajitschek et al. 2006, Ricankova et al. 2007, Cheetham et al.
2008, Senar et al. 2013), the role that familiarity plays in mate choice copying is unknown.
Based on the benefits of copying individuals with shared experiences, the potential for reduced aggression, and studies of copying in non-mating contexts, we hypothesized that females will use social information more when females are familiar with one another. To test this hypothesis, we conducted preference trials using adult female American goldfinches as subjects. A previous study demonstrated that goldfinches will engage in mate choice copying (Chapter 3). We established two treatments, one treatment provided the observer female with the opportunity to copy the mate choice of a familiar female and the other treatment allowed the observer female to copy the mate choice of an unfamiliar female. We predicted that a female would spend more time with a less preferred male after observing that male with a familiar female compared to an unfamiliar female. In addition, we predicted that the effects of familiarity would increase as females spent more time together.
66 METHODS
Study System
The American goldfinch (Spinus tristis) is a small songbird that is abundant and widely distributed across temperate North America. Typical habitats include weedy fields, orchards, and gardens where they feed in pairs or small groups in spring and during the breeding season
(McGraw and Middleton 2009). Goldfinches are sexually and seasonally dimorphic. Male goldfinches express multiple conspicuous sexual traits, which vary among individuals and for which females are known to have preferences (Johnson et al. 1993). Additionally, goldfinches are gregarious year-round and are not known to defend food sources nor breeding territories
(McGraw and Middleton 2009). They are mostly socially monogamous (McGraw and
Middleton 2009) and will engage in mate choice copying (Chapter 3). This social nature of the species makes them well suited to a study exploring the role of social influences on variation of female mating preferences.
Trapping and Housing
All procedures and facilities for this study were approved by the following: The Ohio
State University Institutional Animal Care and Use Committee (Animal Assurance #A3261-01,
Protocol #2012A00000071), Fish and Wildlife Service Scientific Collecting Permit
(#MB71738A-0), Ohio Division of Wildlife Scientific Collecting Permit (#17-285), Federal Bird
Banding Permit (#22688), Ohio Division of Wildlife Banding Permit (#18-105).
Twenty-four wild adult female American goldfinches were trapped and held in captivity for the duration of this study. Trapping locations were Waterman Agriculture and Natural
67 Resources Laboratory Complex on The Ohio State University campus (Columbus, OH,
40°00’39”N 83°01’51”W), Highbanks Metro Park (Lewis Center, OH, 40°09’01”N
83°02’01”W), and The Dawes Arboretum (Newark, OH, 39°59’43”N 82°25’18”W). Custom- built traps were used to capture birds. The traps were made of 1.27 cm wire mesh (hardware cloth) and measured approximately 38 cm W x 38 cm L x 71 cm H. The traps were designed with several tunnels and larger openings (“windows”) that allowed the birds free access to a feeder that hung inside (Fig. 1).
Traps were put out at the various locations from approx. 2–6 weeks in advance of actual trapping and left 24/7. Trapping of birds only took place when a member of the research team was present. Otherwise, the trap functioned essentially as a bird feeder where the birds entered and exited freely. When trapping, the “windows” were covered so that birds attempting to reach the feeders could only enter through the tunnels and, once inside, escape through the “windows” was prevented. Birds in the trap were then caught by hand.
Male goldfinches were banded and immediately released; female goldfinches were held for study. Banding consisted of marking each bird with a federal metal band on one leg and two plastic coloured bands on the other leg. The 24 females used in this study were trapped during
July 2016. Twelve of them were trapped at Highbanks Metro Park, ten were trapped at The
Dawes Arboretum, and two were trapped at the Waterman Agriculture and Natural Resources
Laboratory Complex. Eight of the females were second-year birds (hereafter “younger”) meaning that this was their first breeding season. The remaining sixteen females were after- second-year birds (hereafter “older”) meaning that this was their second or later breeding season.
Birds were aged using standardized plumage identification techniques (Pyle 1997).
68 Female goldfinches used in this study were housed indoors in Aronoff Laboratory on The
Ohio State University campus. Temperature (and humidity) was checked at least daily to be between 17° and 29° Celsius (35% average relative humidity). Photoperiod was set to match
July’s peak breeding season sunrise/sunset times. Pairs of birds were kept in standard bird cages.
Housing the birds in pairs allowed for social interaction with other females during the period of captivity. In five years of housing birds in this manner, no injuries or serious aggressive interactions between cagemates have been observed. Standard husbandry procedures were performed daily. A variety of bird seeds (sunflower, safflower, thistle, millet, etc.) and fresh water were provided ad libitum. A commercially available multi-vitamin supplement for birds and high-calcium grit were also provided. Birds were kept in captivity for approximately 60 days. This length of captivity was necessary to ensure proper separation of trials to avoid problems related to habituation to the trial arena, to adjust photoperiod to match wild conditions at release, and to assist with coordinating of capture and release dates, which often needed to be adjusted due to weather conditions. Birds had ample opportunities to exercise their flight muscles when in the trial arena (as full flight was possible) so that they were healthy and fully capable of flight upon release. At the completion of the study, 23 females (excluding one female that died while in captivity) were successfully released at their site of capture.
Experimental Design
To manipulate familiarity, we split the captive population into two unfamiliar groups with an opaque curtain in the housing room. Additionally, females were assigned to the two unfamiliar groups based on capture location, further ensuring that members of one group will have had no previous knowledge of members from the other group. Although the females on
69 opposite sides of the barrier were still able to interact acoustically with one another (due to housing space constraints), visual interactions were prevented. Cages on each side of the curtain were rearranged daily to ensure that individuals could not be localized to a single location.
Females from opposite sides of the curtain are considered unfamiliar females. Physical interactions were only able to occur between cagemates (birds are kept in pairs). Cagemates are considered familiar females. To ensure familiarity, cagemates were housed together for a minimum of 26 days before starting trials. Senar et al. (1990) determined that 20 days of cohabiting in the same cage was enough to establish familiarity in siskins (Spinus spinus), a close relative of goldfinches.
Each female was the subject (i.e., the observer female) of two preference trials and served as a demonstrator female for two preference trials. One female died before the completion of her second preference trial. Trials for each female were separated by at least five days.
The trials were conducted in a custom-built arena consisting of three sections: a center and two identical side sections branching off from opposite ends of the center (Fig. 2). Different male taxidermy models were placed in each of the side sections for simultaneous presentation to the observer female. The use of models as “substitutes” for live birds is well established in the literature (e.g., Höglund et al. 1995, Murphy et al. 2014) and helps to control for behavioural differences that might be exhibited among live males.
In each trial, we presented the female with a choice between two male taxidermy models.
To give the appearance of “singing,” a goldfinch song recording was played from behind each model (Fig. 2) during each phase of each trial (see Supplemental Material for more details on the songs). Four male taxidermy models were used in this study and were randomized across
70 females. Over the two trials, each female saw three of the four models but the pairings of males differed for each trial. All four male models were older birds.
To reduce stress from handling and introduction to a new environment, birds were first allowed to acclimate to the arena. During the acclimation period, the female’s movements were restricted to the center section of the arena. The acclimation period lasted for a minimum of 30 minutes or until the bird was observed exploring, preening, sleeping, bathing, or feeding, whichever came last. If a bird did not meet these criteria within 60 minutes, the trial was terminated. All birds successfully met the criteria for all trials. Opaque barriers blocked the females’ view of the males. No songs were played during this time.
Following the acclimation period, each trial consisted of three phases: pre-test, observation, and post-test (Fig. 10). At the start of each phase, opaque barriers blocking the two side sections were raised and the female was allowed to move freely about the entire arena except for a small area containing the models. If females did not visit both side sections of the arena within 60 minutes of the barriers being raised, the trial was terminated. After both side sections had been entered by the female, she was observed for 30 minutes.
71
Figure 10 Diagram depicting the relationship between trial, phase, and treatment. Treatments took place during the observation phase of each trial. During the pre-test and post-test phases, both the more preferred and less preferred males are alone. Vertical bars within each box represent the separation of the 3 different areas of the arena
– the center where the focal female is placed and the 2 ends of each side section of the arena where the models are located. F=familiar, UF=unfamiliar. ♂+ = the more preferred male, ♂- = the less preferred male.
We used the pre-test phase to determine the female’s initial preference between two males. The pre-test phase was viewed live and time spent in each section of the arena was measured in real time using JWatcher. The more preferred and less preferred males were determined by calculating the amount of time the female spent in each side section of the arena.
The male in the side section of the arena where the female spent the most time, of time spent in either side section, was designated as the more preferred male and the other male was designated as the less preferred male. These designations did not change in subsequent phases (i.e., the less preferred male from the pre-test is referred to as the less preferred male throughout, even if the female’s preferences changed).
72 To test whether a female is more likely to copy the mate choice of a familiar rather than unfamiliar female, we lowered the barriers and confined the female to the center of the arena while one of two observation treatments, randomized among females, followed (Fig. 10). We placed next to the less preferred male either a familiar female (i.e., the observer female’s cagemate) or an unfamiliar female (i.e., from the opposite side of the opaque curtain in the housing room). Demonstrator females were placed in small custom-built cages next to the less preferred male. An identical empty cage was placed next to the more preferred male. Once the demonstrator female for the observation phase was in place, the barriers were raised and females were allowed to move about the entire arena. Following the observation phase, the barriers were lowered and the observer female was again restricted to the arena’s center. The demonstrator female and both cages were removed. For the post-test, the barriers were raised and the female was again permitted to move about the entire arena.
To measure time spent in each section of the arena, all trials were recorded using a network camera with live video feed placed directly overhead and centered above the arena.
Recorded trials were reviewed using Windows Media Player 12.0.7601.18741 (Microsoft
Corporation, 2009) and time spent in each section of the arena (center and both side sections) was calculated for the observation and post-test phases using JWatcher v1.0 (available from http://www.jwatcher.ucla.edu/).
Statistical Analysis
To measure the change in time spent with the less preferred male, the dependent variable was the difference in the proportion of time spent with the less preferred male from the post-test to the pre-test phase. The proportion of time spent with the less preferred male was calculated as
73 the time spent with the less preferred male divided by the time spent with either male (i.e., not including time spent in the center). This value was calculated for all of the three phases of a trial. Visual inspection of Q-Q plots along with non-significant Kolmogorov-Smirnoff tests indicated that this variable was normally distributed. Additionally, non-significant Levene’s tests showed that the data met the assumption of equal variance.
We used a generalized estimating equation with a normal probability distribution and identity link function to test our prediction that a female goldfinch will increase the proportion of time spent with a less preferred male more after observing that male with a familiar female compared to an unfamiliar female. The difference in the proportion of time spent with the less preferred male over time spent with either male from the pre-test to the post-test phase was the dependent variable. The individual female was included as a subject variable and treatment was included as a within-subject variable. The model included the main effects of treatment, bird age, and trial order and all interactions.
For the familiar female treatment, we used regression to determine if the difference in the proportion of time spent with the less preferred male after observing that male with a familiar female could be explained by the length of time (in days) that the observer and demonstrator females had been housed together.
The critical value for alpha (α) for all tests was set at 0.05. All analyses were performed using SPSS v25 (IBM Corp., Armonk, NY, USA).
RESULTS
Several analyses were completed to test whether the observed results could be explained by any inherent biases related to the arena, the song recordings, or any of the taxidermy models.
74 A binomial test showed no side bias related to the arena with females in 55% of the trials preferring the male model on one side and 45% preferring the male model on the other side
(Z=26.000, N=47, P=0.560). We checked for variation in unresponsiveness (defined as the time it took for the bird to visit both side sections of the arena to start the pre-test phase) that may have been due to the song recordings with a generalized estimating equation and found no
2 significant effect of song (Wald Χ 4=3.952, P=0.413). For the four male models, we looked at whether any of the models was designated more often as the less preferred male. A one-sample
Chi-square test showed that no one model was significantly less preferred over any other model
2 (Χ 3=4.489, P=0.213).
Females increased time spent near the less preferred male more when he was paired with a familiar female than paired with an unfamiliar female. There was a significant effect of treatment on the difference in the proportion of time spent near the less preferred male from the pre-test to the post-test phase (Table 5), with a larger increase after he was observed near a familiar female goldfinch than when he was observed near an unfamiliar female goldfinch
(P=0.040) (Fig. 11). Across treatments, in 79% of the trials (37 of 47), females increased time spent near the less preferred male after observing him with another female.
75 Table 5 Generalized Estimating Equation to examine the effects of treatment, bird age, and trial order on the difference in the proportion of time spent with the less preferred male over time spent with either male from the pre-test phase to the post-test phase. Subject variable is the individual female and within-subject variable is the treatment.
Model Effect Wald Χ2 Df Sig.a Treatment 4.210 1 0.040 Bird Age 0.359 1 0.549 Trial Order 0.992 2 0.609 Treatment*Bird Age 0.910 1 0.340 Treatment*Trial Order 2.262 2 0.323 Bird Age*Trial Order 0.497 2 0.780 Treatment*Bird Age*Trial Order 1.077 2 0.584 a Significant results are in bold.
76
Figure 11 The difference in the proportion of time spent with the less preferred male over time spent with either male from the pre-test phase to the post-test phase based on the treatment. Treatment is the bird (familiar or unfamiliar female) observed with the less preferred male during the observation phase. N=24 for the familiar female treatment and N=23 for the unfamiliar female treatment. Columns represent the mean. Error bars represent 95% CI.
2 *=significant at P<0.05 (Generalized Estimating Equation, main effect=treatment, Wald Χ 1=4.210, P=0.040).
For the familiar female treatment, the difference in the proportion of time spent with the less preferred male from the pre-test to the post-test phase did not change with the length of time
(in days) that the observer-demonstrator pairs had been housed together (F1=0.069, P=0.795)
(Fig. 12).
77
Figure 12 The relationship between the length of time (in days) that the observer-demonstrator pairs were housed together and the difference in the proportion of time spent with the less preferred male over time spent with either male from the pre-test phase to the post-test phase for the familiar female treatment. N=24. R2=0.003. Error bars represent 95% CI. (F1=0.069, P=0.795).
DISCUSSION
Our results supported the hypothesis that females are more strongly influenced by the choices of familiar females. As predicted, we found that female American goldfinches increased the proportion of time spent with the less preferred male more after observing him with a familiar female than with an unfamiliar female. While effects of familiarity have been found for other types of social learning, we are unaware of any studies that have examined the effects of
78 familiarity on mate choice copying. In other social learning paradigms, guppies (Poecilia reticulata) completed a food-finding task significantly faster when learning from familiar demonstrators than from unfamiliar demonstrators (Swaney et al. 2001). Deer mice (Peromyscus maniculatus) were more likely to self-bury in the substrate to avoid biting flies (Stomoxys calcitrans) after having observed a familiar or related demonstrator self-bury than an unfamiliar or unrelated demonstrator (Kaveliers et al. 2005). Valsecchi et al. (1996) found that food preferences of Mongolian gerbils (Meriones unguiculatus) were only transmitted between demonstrator and observer if the two were familiar or related to each other (but see Galef et al.
1998). Effects of familiarity seem to be a robust theme spanning a wide variety of social learning situations. Our results that familiarity among females influences mate choice copying adds to this diversity.
One explanation for our results is that females’ behavior changed more after observing familiar females because information about potential mates is more readily learned from familiar demonstrators. For example, Nicol and Pope (1994) found that the number of hens watching a demonstrator perform was higher for familiar, socially dominant demonstrators than for unfamiliar demonstrators. An observer is more likely to have shared experiences in similar environments with a familiar individual, making the familiar individual a more effective demonstrator. Behavioural coordination in time and space affords the observer its best chance at acquiring detailed information from the demonstrator (Coussi-Korbel and Fragaszy 1995).
Shared experiences and environments provide greater opportunities for this coordination to occur, so that information is more effectively transmitted from demonstrator to observer.
An alternative explanation for our results that females are more likely to copy the mate choice of a familiar individual than an unfamiliar one is that familiarity may also play a role in
79 reducing female-female competition. The effect of familiarity on male-male competition is well documented. Familiarity is key in the relationships among neighbors (Bradbury and
Vehrencamp 2011). The “dear enemy” hypothesis predicts that neighboring territorial conspecific males are less aggressive toward one another than towards an unfamiliar intruder.
This is generally the case because an unfamiliar intruder represents a greater threat to the territory owner than a neighbor with whom boundaries have already been “negotiated”
(Bradbury and Vehrencamp 2011). Male Turkish hamsters (Mesocricetus brandti) housed together exhibited reduced aggression compared to unfamiliar hamsters (delBarco-Trillo et al.
2009). Little is known, however, about the effects of familiarity on female-female competition.
In a study of meadow voles (Microtus pennsylvanicus), pairs of familiar females expressed significantly fewer agonistic behaviors towards each other than pairs of unfamiliar females
(Ferkin 1988). Similarly, female rat-like hamsters (Cricetulus triton) familiar with one another were less aggressive than those unfamiliar with one another (Zhang et al. 2001). Resident females can be highly aggressive towards other females (Slagsvold and Lifjeld 1994) and have even been reported to disrupt extrapair copulations with direct physical aggression (Wagner
1992, Jennions and Petrie 1997). By copying the mate choice of a familiar female, the copier may be reducing the risk of aggressive encounters with the male’s existing mate.
We expected that the effects of familiarity would become stronger the longer that females were together, leading to enhanced social learning and a greater tendency to copy. As cagemates were together for longer periods of time, we began to see bouts of begging and allofeeding attesting to the growing strength of their social relationship (D. Bolen, pers. obs.). However, we found that the length of contact between the observer-demonstrator pairs of familiar females did not significantly influence the amount of the increase in time spent with the less preferred male
80 from the pre-test to the post-test phase. Familiarity among the closely related siskin is established in 20 days of cohabitation (Senar et al. 1990). One possible explanation is that once familiarity is established (i.e., meets some threshold value), additional time together does not correlate with an ever-increasing tendency to copy the familiar individual. Such a threshold could affect the speed of transmission of social information through social groups with faster transmission occurring only after some level of familiarity or group stability is attained. When this type of directed social learning exists, social information will spread through the group at differing rates and to differing extents promoting variability of behaviour among members of that group (Coussi-Korbel and Fragaszy 1995).
Familiarity is a cause and a consequence of the social organization of species. In many groups, individuals preferentially interact more with some than with others (e.g., Croft et al.
2004, Lusseau and Newman 2004, Krause et al. 2010). In non-mating contexts, group structure
(e.g., social network) has been shown to strongly influence transmission of social information
(e.g., Farine et al. 2015, Firth et al. 2016). Previous studies (Chapter 3) have shown that social encounters with other females can alter a female’s mate choice preferences. Because female mate choice is a key influence on the evolution of male traits, this suggests an important potential role of female-female social relationships on male reproductive success and the evolution of male characteristics.
SUPPLEMENTAL MATERIAL
One of five goldfinch song recordings were played during each trial to give the appearance that the male models were “singing”. Three recordings, acquired from the Macaulay
Library at the Cornell Lab of Ornithology, were made in Maryland (May 1998), Tennessee (June
81 1994), and California (April 1991). The remaining two recordings, acquired from the Borror
Laboratory of Bioacoustics at The Ohio State University, were both made in Ohio (May 1956,
April 1957). A section of continuous male goldfinch song was taken from each recording. Each section was unaltered, with the exception of being put through a high pass filter at 1,000 Hz to remove low frequency noise. The two Borror Lab recordings were also put through a low pass filter at 20,000 Hz to remove high frequency noise. Each section of song was repeated two or three times with 2-4 minutes of silence added after each section so that the playback alternated between periods of song and periods of silence. Using Audacity 2.0.3 (computer software audio editor, available from http://audacity.sourceforge.net/), the resulting playbacks (average of 16 minutes) were set to loop continuously during each phase of each trial.
The pairing of playback recordings with trials was randomized among females, and each female heard each recording only once. Playback recordings used when a female was acting as the demonstrator were not used when a female was the observer bird. To control for differences in preference between two males based on song, both males being presented to the female during each of the phases of a trial were singing the same song. However, to prevent it from sounding like they were singing in unison, the beginning of playback for the males was offset by 30 seconds so that for the duration of the playback loop there were times when each male was singing by himself and times when their singing overlapped. Additionally, playbacks were constructed so that males would alternate between which started singing first after each period of silence for as long as the playback looped. This controlled for any preference biases that may be directed toward the male that was heard singing first.
82 Chapter 5. CONCLUSION
Much of the focus of female mate choice research has been on how female preferences affect reproductive success of males and the evolution of male traits; less is known about the intrinsic variation in female preferences and how context-dependent variation affects a female’s mate choice decisions. In order to begin to appreciate the complexity of mate choice decisions and how those patterns contribute to the form of a species, we must understand both the consistency in expression of female preferences and factors that may influence her to alter those preferences. In this project, I looked at three aspects of variation in female preference. First, I determined the variability (or consistency) of female preference for song length by measuring repeatability. Next, I looked at mate choice copying to see if a female’s preference for a previously less preferred male could be influenced by the presence of another female. Finally, I examined whether a female is more likely to copy the mate choice of another female if they are familiar or unfamiliar with one another.
In Chapter 2, I predicted that repeatability of preference for song length would be high and that females would prefer longer songs. I found no repeatability in preference for song length but did find an overall preference for shorter songs. Several factors might have contributed to the lack of repeatability, including the experimental arena design, the motivational state of the females towards mating, and a strong side bias. The preference for shorter songs was unexpected as numerous studies have reported that females prefer males that sing longer songs.
Additionally, male song length is often an indicator of male quality, such that higher quality
83 males sing longer songs. This is the first study that I am aware of that has demonstrated preference for short songs. I suggest that the odd finding that females prefer shorter songs may have been a result of the editing of the songs for playback. Lack of repeatability and, therefore, high within-individual variation indicates that preference for song length may be weak when measured as an independent trait. If context is an important factor in determining female preferences, then I might expect that in the absence of those cues, within-individual variation will be high as I found in this study. I suggested that context, including the social environment, may be important in altering the expression of female preferences.
Knowing the extent to which females differ consistently in expressing their preferences can potentially tell us not only how a particular male trait evolved but what selective forces are acting to maintain it. For example, among-individual variation in repeatability of preferences for particular traits might explain how multiple redundant sexual traits are evolved and maintained.
If within-individual variation in preference is high for a particular trait, it might indicate that preference for that trait alone is weak, but it doesn’t necessarily mean that that trait is unimportant or uninformative in evaluating potential mates. That trait might function as part of a multimodal signal or it may serve to enhance detection of other signals. Determining repeatability for male sexual traits such as song length is important because it can tell us about the relative importance of various male sexual traits in female choice. If we want to understand the evolution of male sexual traits, then we need to know which traits females are actively selecting for and which traits might be products of forces such as pleiotropy.
In Chapter 3, I assessed how the choices of other females influence female preference.
Mate choice copying occurs when a female is more likely to choose a male as a mate if he has been observed with other females. Mate choice copying for individual males has not previously
84 been found in a socially monogamous species other than captive zebra finches and even then results have been mixed. I predicted that a female will increase her interest in a less preferred male after observing that male with another female. I found that the difference in the proportion of time spent with the less preferred male increased more after having observed him with another female goldfinch than with a male goldfinch or female house finch. It is unclear why mate choice copying would be observed in a socially monogamous species when there are direct benefits associated with choosing an unmated male as a mate. I suggested that copying may occur when choosing extrapair mates but not the social mate. In the context of extrapair mating, using readily available social information, such as the mate choice decisions of other females, may be an effective decision-making strategy. Therefore, despite being a socially monogamous species, goldfinches appear to use copying when choosing extrapair mates.
In Chapter 4, I examined how social relationships among females might make copying more likely. Copying can be advantageous in that it allows the copier to avoid the costs associated with asocial learning. However, the copier also runs the risk of relying on unreliable or inaccurate information. Because familiar females are likely to share similar environments and experiences, a female may benefit more from copying a familiar rather than an unfamiliar female. I predicted that females would spend more time with a previously less preferred male after observing him with a familiar rather than an unfamiliar female. I found that time spent with the less preferred male increased more when he was paired with a familiar female than paired with an unfamiliar female. I concluded that social learning may be facilitated by familiarity and that, in the context of extrapair mating, copying familiar females may serve to lessen aggression from the resident female. While effects of familiarity have been found in other contexts, I show here that familiarity influences copying the apparent mate choices of others.
85 Studies of sexual selection can offer potential explanations for the evolution of sexual dimorphism, conspicuous ornaments, and mating systems in a wide range of taxa. For example, one of the effects of mate choice copying may be the evolution of genetically polygynous mating systems. Females may select a polygynous male because they have similar preferences for the male’s traits, but they may also be selecting the same male because they are copying the mate choice of each other. Alternatively, monogamy may result if females actively avoid mating with already mated males. If female avoidance is strong enough, monogamy can result despite a male’s tendency to be polygynous. Either way, female preference, whether for mated or unmated males, may influence a species’ mating system. Mate choice copying is not expected to be found in monogamous systems because the costs incurred probably outweigh any benefits received (Vakirtzis and Roberts 2010). Evidence for mate choice copying in monogamous species has been mixed. In this study, I offer a potential explanation for why mate choice copying can be seen in a socially monogamous mating system. That is, monogamous females may copy the mate choice of others when seeking extrapair copulations. This affords them the opportunity of mating with high quality mates while retaining the benefits provided by their social mate.
Female mating preferences are heritable (Majerus et al. 1982, Bakker 1993). However, when mate choice copying or other forms of social learning about mates exist, mating preferences can also be transmitted culturally. Cultural transmission of preferences can occur vertically (parent to offspring), horizontally (among individuals in a cohort), or diagonally
(where immature females observe older, unrelated females) (Kirkpatrick and Dugatkin 1994) resulting in the spread of a preference through a population at a faster rate than if the preference was transmitted strictly via inheritance (Brooks 1996). This non-genetic transmission of female
86 preferences can act on male ornamentation (Gibson and Höglund 1992, Kirkpatrick and
Dugatkin 1994), as well as increase the variance of male mating success (Wade and Pruett-Jones
1990), making it an important evolutionary process. Copying can result in more rapid fixation of the male ornament on which the preference is based. It can also lead to the loss of all but the most common male traits (on which a preference is based) in a population (Brooks 1996). This occurs because copying conveys a positive frequency-dependent selective advantage for the most common male type since female preference (due to copying) for that male type will be strongest.
Simply put, copying acts to strengthen female preferences for the male type that is already most preferred (Kirkpatrick and Dugatkin 1994). I have shown that the presence of another female can influence a female’s mating preference for previously non-preferred males. The scope of this study did not go so far as to follow the females all the way through to actual mate choice and reproduction, but I have demonstrated that the potential exists for a female to be influenced into changing her choice of mate. Additionally, I have shown that familiarity among females may affect the likelihood that copying will occur. Familiarity may also affect the potential for and rate of social learning, as well as the transmission of information through a social group.
Sexual selection on male traits may depend heavily on characteristics of the physical and social environment that influence female preference and choice. The female’s social environment might be one such context. In Chapters 3 and 4, I present results of experiments varying social context of choice and find strong influences of the behaviour of other females on apparent preferences. The potentially vital role that a female’s social life may play in the variability of preferences and, ultimately, her decision-making should not be overlooked
(Jennions and Petrie 1997, Westneat et al. 2000). Because female mate choice is a key influence
87 on the evolution of male traits, this suggests an important potential role of female-female social relationships on male reproductive success and the evolution of male characteristics.
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