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MPIDR WORKING PAPER WP 2010-032 NOVEMBER 2010
To care or to fi ght: must primate males choose?
Daniel A. Levitis ([email protected]) Laurie Bingaman Lackey
This working paper has been approved for release by: Alexander Scheuerlein ([email protected]), Deputy Head of the Laboratory of Evolutionary Biodemography.
© Copyright is held by the authors.
Working papers of the Max Planck Institute for Demographic Research receive only limited review. Views or opinions expressed in working papers are attributable to the authors and do not necessarily re ect those of the Institute. 1 To care or to fight: must primate males choose?
2
3 Daniel A. Levitis1,2 and Laurie Bingaman Lackey3
4 1Max Planck Institute for Demographic Research
5 Laboratory of Evolutionary Biodemography
6 Konrad-Zuse-Straße 1
7 18057 Rostock Germany
8 Email: [email protected]
9
10 2Museum of Vertebrate Zoology
11 University of California, Berkeley
12 3101 Valley Life Sciences Building
13 Berkeley, CA 94720-3160 USA
14
15 3International Species Information System
16 2600 Eagan Woods Drive, Suite 50
17 Eagan, MN 55121-1170 USA
1 18 Females in all mammalian species care for their offspring, while most mammalian males
19 do not. This failure of paternal investment is generally explained in terms of a trade-off
20 between paternal care and mating competition. While there has been great interest in the
21 optimal pattern of investment in paternal care versus mating effort, comparative evidence
22 that such a trade-off exists has not been published for any large group of mammal
23 species. We employ comparative data on primates to test for such a trade-off. Across
24 primate species, the degree to which males engage in direct care of young is inversely
25 related to levels of overt male-male conflict, and to canine dimorphism, a morphological
26 measure associated with male-male conflict. When phylogeny is taken into account, there
27 is no significant relationship between sex-biased longevity and whether males engage in
28 care, implying that investment in care and investment in competition are functional
29 alternatives to each other. Males of most primate species engage in either intensive direct
30 care, or intense or frequent intrasexual competition, but not both. The hypothesis that
31 investment in care and in intrasexual conflict are alternative strategies is strongly
32 supported.
33
34 Keywords: paternal care, primates, tradeoffs, reproductive strategies
2 35
36
37 1. Introduction
38
39 It is frequently argued (e.g., Clutton-Brock 1989; Gubernick & Teferi 2000; Trivers
40 1972) that the high prevalence of males who do not care for their young is driven by the
41 need to partition limited resources. Males of many species may gain higher fitness by
42 investing their reproductive effort in competing with other males for access to females
43 rather than caring for existing young. Similarly, an existing tendency toward paternal care
44 may limit the resources males can dedicate to fighting with each other. However a trade-
45 off between paternal care and male-male conflict has been demonstrated for few groups
46 of species (Tanganyikan cichlid fishes (Gonzalez-Voyer et al. 2008) and shorebirds
47 (Thomas & Székely 2005)), and across no large group of mammals. It is particularly
48 surprising that such a relationship has not been demonstrated in primates, both because
49 there has been considerable interest in the evolution of paternal care in primates (Buchan
50 et al. 2003; Charpentier et al. 2008; Kleiman 1985; Tardif 1994; Wright 1990) and
51 because there is a large and fruitful comparative literature on primate life-history
52 evolution (e.g., Bronikowski et al. 2002; Kappeler & Pereira 2003; Lee 1999; Thoren et
53 al. 2006). We present comparative evidence bearing on the question of whether the males
54 of a primate species must choose to help raise young or to fight with each other for access
55 to mates, but cannot do both. We further examine whether this choice influences sexual
56 dimorphism in longevity, complicating the structure of the tradeoff.
3 57 A casual survey of primate species reveals a negative correlation between two
58 important aspects of male reproductive effort: paternal care and male intrasexual conflict.
59 In large groups of primates, particularly the Aotidae and Callitrichidae (Kleiman 1985;
60 Nowak et al. 1999), males provide extensive care to young and overt conflict between
61 males is rare. In others, such as the Cercopithecids, paternal care is absent or minimal,
62 male-male conflict is intense, and morphological dimorphism in size and dentition
63 (correlates of intrasexual conflict Leutenegger & Kelly 1977; Mitani et al. 1996; Plavcan
64 2004) are generally large (Plavcan & van Schaik 1992; Plavcan & van Schaik 1997). We
65 focus on these two aspects, although other forms of competition and investment (e.g. in
66 sperm competition or influencing female choice) may also be important.
67 The choice of whether to dedicate one’s time to fighting or to caring potentially
68 conflates two of the most central life-history trade-offs: the balance between reproductive
69 rate and mortality risk reduction (Cichon 1997; Partridge 1987; Williams 1957; Williams
70 1966), and between offspring quantity and offspring quality (Clutton-Brock 1991; Lack
71 1954; Smith & Fretwell 1974; Walker et al. 2008). In primates intrasexual mating
72 conflict bears considerable mortality costs (Smith & Jungers 1997). Therefore the
73 outcome of the trade-off between male care and mating competition may be influenced
74 by the fact that one choice (care) allows for greater longevity than the other.
75 Allman et al. (1998) argue that in primate species where paternal care is
76 prevalent, the ratio of female to male longevity is lower than in other primates.
77 Caretakers may live longer because they experience more intense selection against
78 premature mortality (Plavcan et al. 1995). A caretaker who dies loses not only the ability
79 to produce future offspring, but also some portion of the fitness prospects of extant
4 80 offspring, who are deprived of the resources which otherwise would have been
81 transferred to them (Chu et al. 2008; Lee 2003). In such a situation, males would need to
82 balance increased production of offspring on the one hand against the combination of
83 higher offspring quality and higher longevity on the other, complicating the selective
84 calculus.
85 In models of this decision making process (e.g., Kokko & Jennions 2008; Webb et
86 al. 2002), mated individuals face the choice to continue investing in the fitness of current
87 offspring (bearing fitness costs in the form of time, individual quality and mortality risk),
88 or abandoning mate and young to seek new mating opportunities (also incurring costs and
89 risks). The likely payoff in each scenario may depend on several variables, many of
90 which are rarely measured in wild populations. These include the social system, the
91 Operational and Adult Sex Ratios, the need for biparental care, the non-random variance
92 in lifetime mating success and reproductive success for each sex, the certainty of
93 parentage and the relative mortality risks of the two activities. The interactions of these
94 many variables and multiple individuals can lead to strongly counter-intuitive results. For
95 example, Kokko and Jennions (2008), in a recent formal model and detailed discussion of
96 the co-evolution of parental investment and mating competition, found that when
97 multiple traits are allowed to co-vary, increasing the mortality risk associated with a
98 strategy can lead to an increased optimal investment in that strategy, not the decreased
99 investment intuition would tend to point to. They also clarify that where mate
100 competition and parental care consist of the same activity (e.g., where females are more
101 likely to mate with males whom they have observed to be involved fathers) the two goals
102 may cease to be in competition. Due to these complexities, and the possible failure of
5 103 intuition, we argue it is necessary to test for, rather than assume, the trade-off between
104 investment in intrasexual mating conflict and investment in parental care in taxa for
105 which we think this trade-off important.
106 In the current paper we conduct a phylogenetically controlled comparative
107 analysis, focusing on primate males. Approximately 60% of primate genera display no
108 male care, according to an older and probably somewhat high estimate (Kleiman et al.
109 1981), allowing for a robust set of contrasts between caring males and non-caring males.
110 We employ these phylogenetic contrasts to examine the co-evolution of paternal care,
111 male-male conflict and sex-biased longevity in primates. We test the assumption that they
112 are traded-off against each other by examining the predictions that males of each species
113 will tend to invest heavily in care or competition, but not both, or neither; that the
114 correlation between these two types of reproductive effort is stronger than the
115 relationship of either to longevity and that these relationships are phylogenetically robust.
116
117 2. Methods
118
119 For 63 primate species for which longevity dimorphism (see below) and mass
120 dimorphism data (Smith & Jungers 1997) were available, we searched for data on the
121 remaining variables (paternal care, male-male conflict and canine dimorphism). We
122 included in this sample 54 anthropoid primates and 10 strepsirrhines (lemurs, galagos and
123 lorises). While the effect of mating conflict on sexual dimorphism is thought to be limited
124 in strepsirrhines (Plavcan et al. 1995), we had no a priori reason to believe that the
6 125 presence or absence of a trade-off between care and competition would differ between
126 strepsirrhines and anthropoids.
127 Data on paternal care in each of these species were gathered from smaller
128 previous compilations (Allman et al. 1998; Smuts & Gubernick 1992) and their
129 references, and supplemented extensively by a review of the literature. We defined
130 paternal care as acts by breeding males directed toward known or possible offspring (i.e.,
131 no attempt was made to estimate paternal certainty), likely to enhance the survival or
132 status of those offspring, excluding the discouragement of infanticide by conspecifics.
133 We had two reasons for not including protection from infanticide. We could not quantify
134 this effect consistently across species, and infanticide deterrence may result from males
135 excluding other males from access to females. Thus, it may represent investment in
136 mating rather than in care (van Schaik & Kappeler 1997). In this we followed Smuts and
137 Gubernick (1992) who focused on direct, rather than indirect male care. Previous surveys
138 of paternal care in primates either treated this as a dichotomous variable (Smuts &
139 Gubernick 1992) or provided a verbal account of care in each species (Allman et al.
140 1998; Wright 1990). We coded paternal care as an ordered multistate variable because it
141 provided finer distinctions than an artificially dichotomous variable, while allowing for
142 quantitative analysis. We rated each species' paternal care on a scale of 1 to 4 using the
143 following criteria:
144
145 1. No evidence of fathers directing beneficial behaviours toward the young.
146 2. Evidence of limited offspring-directed-activities with uncertain selective effect, such as
147 tolerance of playing.
7 148 3. Evidence of regular paternal involvement likely to enhance survival or status of young.
149 4. Fathers are primary caregivers at some developmental stage.
150
151 For several well-studied species no information regarding paternal care could be found in
152 the literature. In these cases we rated the species as level 1 only if other literature
153 describing the pattern of care and allocare in the species existed, and these studies were
154 conducted under circumstances in which the opportunity existed for paternal care, but
155 none was described. We reasoned that researchers studying the pattern of care in a
156 species are far more likely to record the observation of male care than to mention in
157 publication the lack of such observations (a form of publication bias, Dickersin & Min
158 1993), leading to systematic underreporting of the lack of male care. For 19 species we
159 were unable to reach any confident conclusion regarding paternal care, and considered
160 these to be missing data, leaving us with paternal care classifications for 44 species. We
161 employed data on captive individuals but gave greater credence to observations from the
162 wild.
163 Humans proved a difficult species to classify in this way, in that fathers provide
164 differing amounts of care across societies (Marlowe 2000), and authors disagree as to the
165 importance of this care to offspring. Summarizing across societies and opinions, we
166 classified human paternal care as a 3, meaning that human fathers are clearly important to
167 the success of young but are not the primary source of care (although they may be the
168 primary source of calories and protein, (Kaplan et al. 2000).
169 Data on intensity and frequency of male-male competition were from Plavcan and
170 van Schaik’s (1997) four level ordinal classification of anthropoid primates. These data
8 171 were available for 36 of our focal species. This scheme relies on classifying conflict
172 between males in each species as high-intensity or low-intensity (based on the tolerance
173 of males to sharing space), and as frequent or infrequent (based on the number of males
174 in a group, and other factors influencing how often males are likely to be in proximity
175 with each other). Intensity of conflict is given priority over frequency of contact in
176 ordering the four possible classifications, such that level 1 is low-intensity, low-
177 frequency; level 2 is low-intensity, high-frequency; level 3 is high-intensity, low-
178 frequency and; level 4 is high-intensity, high-frequency. Criticisms of this classification
179 system (Lindenfors 2002), and detailed responses to those criticisms (Plavcan 2004) have
180 been published. Humans were not included in this scheme, but would likely be classified
181 as having high frequency of interaction, and therefore category 2 or possibly 4. As our
182 analysis focused on physical conflict between males, rather than reproductive
183 competition more generally, we did not include data on sperm competition or other less
184 direct forms of competition. We note that testes mass as a portion of male body mass (a
185 proxy for investment in sperm competition) in a collection of primates {Harcourt, 1995
186 #2166}, is correlated with neither level of paternal care (ANOVA, n=27, R2=0.05,
187 F=0.43, P>0.7) nor intensity of male-male conflict (ANOVA, n=25, R2=0.21, F=1.86,
188 P>0.16).
189 Sex specific body mass data for all 63 species were extracted from Smith and
190 Jungers (Smith & Jungers 1997). Data on dimorphism in canine volume for 41 species
191 were taken from Thoren et al. (2006)) and largely based on the compilation of Plavcan
192 (1999). Mass and canine dimorphism data have been used in several studies and have
193 proven to be strong correlates of male-male conflict (Leutenegger & Kelly 1977; Mitani
9 194 et al. 1996; Plavcan 1999; Plavcan 2004; Plavcan & van Schaik 1992; Thoren et al.
195 2006). However, focusing on males did introduce a potential source of error when
196 considering dimorphism. Females are not a fixed basis, around which males evolve, but
197 evolve in their own right and co-evolve with males, influencing dimorphism (Lindenfors
198 2002). However, rather than attempting to control for the influences of female evolution,
199 we left them in place, preferring to underestimate the correlations between the traits we
200 focus on rather than introduce spurious correlations in attempting to minimize existing
201 error. Additionally, and in contrast to previous studies using these data, we did not scale
202 size of teeth to size of body before calculating canine dimorphism. We made this choice
203 because error in estimates of body mass are likely to be proportionately larger than error
204 in dental measurements (Plavcan 2004) , due to the greater effect of environment, season
205 and population sampling on body mass. Controlling for body mass would have
206 transferred this error into canine dimorphism data. Therefore, we took canine dimorphism
207 as an independent measurement of dimorphism that incorporates information on both
208 relative size of males and females and their dentition.
209 Longevity data were from the International Species Information System (ISIS,
210 (Earnhardt et al. 1995), which compiles data from zoos. Discussion of the strengths and
211 weaknesses of ISIS data can be found in (Kohler et al. 2006). Captive primates will
212 reflect evolved capacity for longevity more so than do wild populations, which tend to
213 die younger. The sex experiencing more extrinsic mortality in the wild is expected to also
214 live shorter in captivity, because high extrinsic mortality leads to the evolution of high
215 intrinsic mortality{Austad, 1993 #2167}. Our measure of longevity, parameter Z,
216 represents a near endpoint of the population's capacity for longevity, but excludes the
10 217 right tail of the survivorship distribution so as to avoid potential problems associated with
218 using maximum observed longevity, such as undue influence of outliers and sample-size
219 effects. If the probability of surviving from age zero to each age x is lx, Z was calculated
220 as the smallest integer meeting the condition that:
z ∞
221 ∑lx ≥ 0.95∑lx x=0 x=0
222 Z then is the age by which 95% of total years lived by an average cohort are past.
223 Longevity dimorphism was calculated as (Zfemale- Zmale)/(0.5*( Zfemale+Zmale)).
224 In addition to phylogenetic information, we incorporated into our dataset paternal
225 care data for 44 species, dental dimorphism data for 41 species, male-male competition
226 data for 35 species and data on body mass and longevity for all 63 species. These data are
227 presented in Appendix 2. Each analysis included all species for which the necessary data
228 were available, such that sample sizes vary between analyses. We calculated correlation
229 coefficients based on ANOVAs and contingency analysis performed in JMP 8 (SAS
230 Institute, Cary, NC). In order to control for the effect of male-male competition on the
231 correlation between paternal care and our three measures of dimorphism, we took the
232 residuals of the plot of each measure of dimorphism over male-male competition, and
233 then plotted these residuals against paternal care, testing for significant correlation.
234 Finally, we calculated coefficients of correlation of phylogenetic independent
235 contrasts, and significance values for these contrasts, using the Analysis of Traits module
236 of the phylogenetic analysis software Phylocom (Webb et al. 2008) and the primate
237 section of a recent mammalian composite phylogeny (Bininda-Emonds et al. 2007).
238 Phylocom calculates a statistic, labelled PicR, which gives the coefficient of correlation
239 between independent contrasts (across nodes) in two traits. Using this procedure, we
11 240 assessed the phylogenetically controlled correlation between paternal care and each of the
241 four other variables in the dataset.
242
243 3. Results
244
245 All pairs of variables in our analysis were significantly correlated (p<0.05, Figure 1) in
246 the predicted directions when phylogenetic relationships were not controlled for. The
247 negative relationship between paternal care and level of male-male competition
248 (contingency analysis, r= -0.65, df=28, χ2=26.332, p<0.005) was supported. Longevity
249 dimorphism (Figure 1a) was low, and often negative (males living longer than females),
250 in species classified as paternal care level 4 (ANOVA, df=43, r=-0.53, F=5.12, p<0.005).
251 Similarly, the correlation between mass-dimorphism and paternal care (Figure 1b) was
252 driven primarily by the very low dimorphism of species with level 4 paternal care
253 (ANOVA, df=43, r2=0.57, F=6.37, p<0.005). Species with paternal care classified as
254 levels 3 and 4 had significantly less dimorphic canine teeth (Figure 1c) than those in
255 levels 1 and 2 (ANOVA, df=26, r2=-0.58, F=3.96, p=0.02). We note that most of the
256 species in these analyses with paternal care level 4 were in the family Callithrichidae, and
257 the remainder were in another New World monkey family, Aotidae.
258 Phylogenetic independent contrasts (Table 1) revealed that the correlations of
259 mass dimorphism and longevity dimorphism to paternal care were weak and non-
260 significant once phylogeny was controlled for. The tendency for caring males to be small
261 and short-lived compared to their females was attributable to the strong tendency for
262 Callithrichids and Aotids to have these traits, and was not a general pattern. In contrast,
12 263 canine dimorphism was still strongly negatively correlated with paternal care (males who
264 care more had relatively smaller teeth, PicR=0.527) after controlling for phylogenetic
265 signal. This correlation was stronger than the correlation of paternal care with the
266 behavioural measure of male-male conflict (caring males competing less, PicR=0.423).
267 Most species in our data set displayed high paternal care and low male-male
268 conflict, or the converse (Supplemental Table 1), explaining the significant (and
269 phylogenetically robust) negative correlation between them. All species displaying
270 frequent or primary paternal care (levels 3 and 4) were within the group classified by
271 Plavcan and van Schaik (Plavcan & van Schaik 1992) as having both low-intensity and
272 low-frequency male-male competition (level 1). Concordantly, only one species,
273 Hylobates lar was classified as displaying limited or no paternal care (levels 1 and 2)
274 combined with low-intensity, low-frequency male-male conflict (level 1). Dividing
275 species into the four blocks suggested by this result (paternal care divided between levels
276 1 and 2 versus levels 3 and 4, and male-male conflict divided between level 1 versus
277 levels 2 through 4, Table 2) revealed that our sample of each family of monkeys falls
278 within only a single block. Hylobatidae and Hominidae were each split between two
279 blocks; Hylobates lar is classified as having lower care than Hylobates syndactylus, and
280 Homo sapiens has more paternal care than other great apes.
281
282 4. Discussion
283
284 Our results strongly support the hypothesis of a trade-off between investment in paternal
285 care and male-male conflict in anthropoid primates. We find not only that these factors
13 286 are negatively correlated, and that this relationship is not an artefact of phylogenetic co-
287 correlation, but that male care and male intrasexual conflict seem to be largely
288 incompatible alternatives strategies. Investment in more than rudimentary paternal care
289 and investment in intense male-male fighting appear to preclude each other.
290 This conclusion, while correlational, is reiterated by the strong negative
291 relationship between male care and canine dimorphism, a good indicator of male-male
292 conflict, and one not based on potentially subjective classifications of behaviour. Both
293 behavioural and morphological indicators of male-male conflict are negatively related to
294 paternal care, and this relationship cannot be explained away as phylogenetic signal.
295 Unexpectedly, the same is not true for mass dimorphism or longevity
296 dimorphism. The apparent correlation of these traits with paternal care arises through the
297 fact that male Callitrichids and Aotids are unusually caring and unusually long-lived and
298 small relative to their female counterparts. Including the members of these two families
299 in analysis as independent samples portrays correlations which are not supported by study
300 of independent contrasts. This does not imply that the unusual traits of males in these two
301 families are unrelated to each other, but does suggest that these relationships are not the
302 rule among primates generally. We note that a previous study (Allman et al. 1998) which
303 argues for a relationship between paternal care and longevity dimorphism in primates
304 relies heavily on Callitrichids and Aotids to reach this conclusion, and does not explicitly
305 consider phylogenetic relationships. A similar study of mammals more broadly (Clutton-
306 Brock & Isvaran 2007) employed phylogenetic controls for other analyses, but not in
307 examining the relationships between longevity to paternal care or male-male competition
308 levels.
14 309 The lack of a robust relationship between longevity dimorphism and paternal care
310 bears on the central question of this paper, the trade-off between care and mating conflict.
311 If investment of time and resources is partitioned between survival and reproduction, and
312 investment in reproduction is further partitioned between increasing quantity of offspring
313 and increasing the quality of offspring, these two partitions are independent only if the
314 choices made in one do not influence the optimal outcome in the other. Insofar as male-
315 male competition is an investment by males in quantity of offspring, and care is an
316 investment in quality of offspring, our data suggest that this partition does not strongly
317 affect overall investment in reproduction versus longevity. If it did so, we would expect
318 to find evidence for a relationship between longevity dimorphism and paternal care. The
319 lack of such a relationship also supports the notion that paternal care in primates, at least
320 when intensive (levels 3 and 4 as we defined them) truly is paternal investment. If the
321 costs to males associated with providing care were systematically lower than those
322 associated with male-male-competition, we would expect species pursuing these
323 strategies to evolve different longevity dimorphisms. This finding is reinforced by the
324 observation that the important division in paternal care is between ‘little’ and ‘lots’,
325 rather than ‘none’ and ‘some.’ Occasional and incidental care need not be costly and
326 therefore need not interfere with fighting for mates.
327 The lack of this interaction with longevity also bears on another persistent
328 question in life-history evolution, whether human females' post-fertile survival is
329 selectively advantageous, and arose due to the extended care they provide to younger kin
330 (Hawkes 2003; Peccei 2001; Williams 1957). Allman et al.'s (1998) paper suggesting that
331 the caretaking sex in primates tends to live longer has been cited as supporting the idea
15 332 that women live longer than men, and longer than their own fertile lifespans, because of
333 kin selection effect associated with their care of older offspring and grandchildren. While
334 the proposed selective mechanism may be important in humans, our data do not support
335 such an effect in primates more broadly.
336 Hylobates lar appear unique in our analysis in that males engage in neither
337 intensive care of young nor intensive male-male competition. Hylobatidae, unlike the
338 various families of monkeys, is not confined to one box of Table 2. This implies that
339 males of Hylobates lar are not investing heavily in either male-male conflict or care of
340 young. We note that their testes to body mass ratio is similar to that of H. syndactylus
341 (Kenagy & Trombulak 1986), which do have significant paternal care, implying that
342 sperm competition is also not what they are investing heavily in. The reproductive
343 strategy of male H. lar may require greater scrutiny in future.
344 The other apparently unusual species in our analysis is our own. While our data
345 suggest that humans are unremarkable in longevity dimorphism (ranked 35th of 63
346 species), mass dimorphism (33rd of 63) and canine dimorphism (12th of 41), we are
347 apparently unusual in engaging in both intensive male care (we estimate level 3) and
348 male-male competition which should probably not be classified as low-intensity, low-
349 frequency (we estimate level 2). While we must always be cautious of thinking ourselves
350 overly exceptional, we guardedly raise the possibility that the trade-off between care and
351 male-male competition may work somewhat differently in humans than in most other
352 primates. If human females tend to choose males who invest in young and female choice
353 influences males' mating access, or the traits which allow males to be good providers also
354 allow them to compete for mates (for example, hunting skill may aid in raising young and
16 355 in securing matings, Gurven & Von Rueden 2006), investment in care and investment in
356 mating competition could be conflated, alleviating the need to invest heavily in one or the
357 other. Separate investment in care and competition, if necessary, could be supported by
358 some other trade-off, such as delayed maturation or extended investment in the young by
359 mothers and grandmothers. Human males may also bring more plasticity to the resolution
360 of this trade-off than do other primates, investing in care or mating effort as conditions
361 and individual status dictate (Hurtado & Hill 1992).
362 The strength of the relationship between paternal care and male-male conflict we
363 have described is surprising, given the wide range of other reproductive tactics and
364 survival tactics that resources could be shunted into, and the wide range of ecologies and
365 social systems represented in our primate sample. While our results leave open the
366 questions of why males can’t both care and fight, why each species partitions
367 reproductive investment in the particular way it does, and why these choices don’t appear
368 to affect sex-biased longevity, they offer a useful system in which to examine these
369 questions. Male primates are apparently forced to choose caring or fighting, these choices
370 appear (given the current system of character coding) to be fairly consistent within
371 families, and there is considerable variation within the primates, a group for which many
372 other comparative datasets in ecology and life-history already exist. Primates are likely
373 our most promising comparative system in which to study why males can’t be both carers
374 and fighters, and how they choose one strategy or the other.
17 375
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21 520 Table 1. Trait correlations based on phylogenetically independent contrasts
Species included, N Correlation, PicR Male-Male Competition 22 0.423* Canine Dimorphism 25 0.527* Mass Dimorphism 39 0.08 Longevity Dimorphism 39 0.08 521 (PicR is the coefficient of correlation between two traits based on phylogenetically
522 independent contrasts . While PicR does not indicate the direction of correlation (positive
523 or negative), each of the correlations described here is negative. PicR values marked with
524 * are significant at p<0.05. )
525
526 Table 2 Primate taxa classified by treating paternal care and male-male competition as
527 dichotomous variables
Low intensity High intensity low frequency or frequency male-male male-male competition competition Atelidae, Cebidae, Pitheciidae, Limited Hylobates lar Cercopithecidae, or no Hominidae paternal (excluding care Homo)
Frequent Hylobates syndactylus, or Homo sapiens primary Aotidae, paternal Callithrichidae care 528 (Levels 2, 3 and 4 of male-male competition are grouped. Paternal care is split between
529 levels 1-2 and levels 3-4. Use of family names indicates that all members of the family
530 represented in our data set fall into the same table cell except where noted. Homo sapiens
531 competition classification is uncertain, but estimated as level 2.)
22 532 Supplemental Table 1. Species classified by level of paternal care and level of male-male
533 conflict
2. Low Intensity 3. High 4. High 1. Low Intensity High intensity Low Intensity High Low Frequency Frequency Frequency Frequency Macaca Cercopithecus fascicularis, neglectus, M. fuscata, Colobus M. mulatta, 1. No guereza, M. silensis, evidence Lagothrix Erythrocebus Mandrillus of lagothricha, patas, Pongo leucophaes, paternal Pithecia pygmaeus, Aloutta care pithecia Saimiri sciureus caraya 2. Limited Ateles offspring- geoffroyi, Gorilla gorilla, Cebus apella, directed- Pan Saimiri Papio activities Hylobates lar troglodytes, boliviensis hamadryas
3. Hylobates Frequent syndactylus, paternal Saguinus care oedipus Aotus lemurinus, A. trivirgatus, Callithrix jacchus, C. pygmaea, 4. Fathers Leontopithecus are rosalia, Saguinus primary fuscicollis, S. caregivers labiatus 534
23 535 Figure 1. Dimorphisms and Paternal Care
536
537 Relationships between paternal care and a) longevity dimorphism, b) body mass
538 dimorphism and c) canine dimorphism. Box plots represent maximum, 75th percentile,
539 median, 25th percentile and minimum for each group. Members of two New World
540 Monkey families (Aotidae and Callitrichidae) are represented as asterisks and other
541 primates are represented as circles.
542 a) Longevity dimorphism and paternal care in 44 primate species. Species in which males
543 are the primary caregivers at some developmental stage (level 4) tend to have males who
544 live longer compared to females (lower longevity dimorphism) than species with less
545 intensive paternal care. This result is primarily due to systematic differences between
546 Aotidae and Callitrichidae and all other primates and is not supported in our analysis of
547 phylogenetically independent contrasts (see text).
548 b) Body mass dimorphism and paternal care. Level 4 male care is also associated with
549 low body mass dimorphism (males relatively small compared to females). Again this
550 result is due to the contrast between Aotids and Callitrichids, and is not phylogenetically
551 robust.
552 c) Canine dimorphism and paternal care. Species in which males provide intensive care
553 (level 3) in addition to those in which they are primary caregivers for offspring at some
554 developmental stages (level 4) exhibit lower canine dimorphism (males' canines being
555 relatively small compared to females') compared to species with limited or no paternal
556 care. This relationship is supported in phylogeneticly controlled analysis (see text).
557
24 558 Figure 1
559 a.
560
561
562 b.
563
564
25 565 c.
566
26