The sociobiological influences on reproductive success and sex ratio manipulation in four orders of zoo-housed mammalia

Collette Monique Thogerson, Purdue University

Abstract

There is an urgent and critical need for drastic conservation measures to be taken to ensure species are not lost to us forever. Captive breeding may soon be the only option for survival of critically endangered species. However, while wildlife populations are imperiled due to anthropogenic influences such as habitat loss and climate change, survival in captivity is threatened by reproductive problems and could potentially be threatened by male biased sex ratios. Using an epidemiological and comparative method approach, we investigated the life history strategies influencing reproductive success and sex ratio manipulation of 222 species from four orders of zoo-housed mammalian using 90 years of breeding at the San Diego Zoo Global. Our results show that across four orders of mammals, dams and sires actively alter their life history strategies to optimize inclusive fitness, by altering life history traits such as age at reproduction, number of offspring, sex ratio and even longevity to win at the game of inclusive fitness and they do so in spite of human attempts at management. We found for both dams and sires, biasing sex ratio towards the more competitive sex is an adaptive reproductive strategy. Individuals who bias towards males leave more grandchildren in total and specifically via the biased sons. Dams who bias towards females have daughters who produce more offspring than dams who do not bias towards females. Lastly we found that while the leading hypotheses developed to explain sex biasing are not universally predictive of which species will bias, inherently biologically characteristics such as sexual dimorphism, maternal investment and group dominance hierarchies can predict whether or not species will have high variance in biasing in a highly provisioned captive environment. These results show that evolutionary legacies of wild species remain detectable even in the captive environment, thus evolutionary theory is not constrained to wild populations and individuals show intra- and inter- species variation in their life history strategies. Specifically, in our first study we found that for both dams and sires, longer lifespans are associated with more offspring and litters (F1,1444 = 32.25, p < 0.0001; F1,440 = 22.46, p < 0.0001, respectively) they have. At higher numbers of litters, per parity litter size for dams is negatively correlated with lifespan (F1,1444 = 9.475, p = 0.0021) and both dams and sires who start breeding later in life, live longer (F 1,1444 = 597.14, p < 0.0001; F1,440 = 228.02, p < 0.0001, respectively), but have fewer offspring in total (F1,1447 = 13.14, p = 0.0003; F1,476 = 15.82, p < 0.0001, respectively). The older a dam is when she starts having offspring, the higher her probability of biasing towards females (F1,1444 = 4.661, p = 0.0309) and dams who bias towards females live longer (F1,1444 = 7.14, p = 0.0076). Those who start a breeding career early have more total offspring but a shorter lifespan. These results demonstrate that clear fitness trade-offs exist in life history strategies, even in an environment with abundant resources and no predation pressure. Despite this, certain individuals across mammalian species are able to capitalize on select life history strategies that enable them to win the genetic lottery by disproportionately propagating the next generation with their genes. We further investigated sex ratio manipulation as a life history strategy. In theory, a parent can maximize fitness by biasing its birth sex ratio in favor of offspring which will outperform those of their peers. Although biased sex ratio is often observed and explained in species-specific terms, the overarching prediction (that offspring belonging to the favored sex produce more grandchildren for their parents), has never been tested in mammals. Therefore, we established third-generation pedigrees to show that in 198 mammalian species both dams and sires consistently bias their sex ratio toward the sex that maximizes second-generation reproductive success. Granddams and grandsires who bias have more grandchildren in total (F1,1427 = 26.45: p < 0.0001; F1,499 = 6.553: p < 0.0108, respectively). Sons of granddams and grandsires who bias towards males have more offspring than sons of those who do not bias (F1,1260 = 194.9: p < 0.0001; F1,468 = 27.53: p < 0.0001). Similarly, daughters of granddams who bias toward females, have more offspring than daughters of females who do not bias (F 1,1390 = 4.891: p = 0.0272). These data clearly demonstrate the ultimate reason why parents control their sex ratio - parents who have cues to the future success of their first generation offspring and bias their sex ratio accordingly have a clear F2 fitness advantage over those who cannot. Therefore, manipulating sex ratio is a widespread and highly adaptive evolutionary strategy in mammals. However, in a captive population under human control, this individually adaptive strategy may be significantly impacting the long term survival of the species as a whole as winners of the genetic lottery do so at others' expense, and a highly successful F1 male over contributes to the next generation at the species-level cost of the loss of genetic variation from the males that fail to breed. Thus the general tendency of captive species to bias their sex ratio demonstrated here (especially in F1 males), combined with the fact that many captive species have male biased sex ratios has the potential to accelerate the loss of genetic diversity from endangered captive-bred species. Lastly we used the comparative method to test if the many hypotheses and post hoc explanations which attempt to explain when and why females might manipulate the sex ratio of their offspring were universal predictors of who would bias across 176 zoo-housed mammalian species, but our results indicate they are not. These hypotheses appear to be species or situational specific. However, we did find that three inherently biological characteristics of mammalian species can predict whether or not dams across species will have variation in their ability to bias their sex ratio. The negative correlation of both sexual dimorphism and maternal investment after weaning with dam variance in sex bias (r = -0.30, F1,162 = 16.33, p < 0.001; (r = -0.24, F1,147 = 9.197, p = 0.003, respectively) is likely because of provisioning. The positive correlation of dominance in the group and dam variance in sex bias (r = +0.24, F1,146 = 9.037, p = 0.003) is likely related to a greater benefit of sons for some individuals. These important characteristics of a species natural history all overlap as key components of the leading hypotheses in sex allocation theory. Thus, while the leading hypotheses may not be able to universally predict who will bias in a highly provisioned population of mammals, certain components of those hypotheses are key features of a species biology that will likely persist as predictors of whether or not females will vary in their ability to bias their sex ratio regardless of the environment.

Degree

Ph.D.

Advisors

Garner, Purdue University.

Subject Area

Ecology|Conservation biology|Behavioral Sciences

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