Determinants of multiple paternity in a fluctuating population of ground squirrels

Abstract

Multiple paternity is common in vertebrates that produce several offspring in the same reproductive bout, but the rate often varies among and within populations. Three primary explanations for this variation have been advanced: null models based on encounter rate of mates, socioecological models dependent on the ability of males to monopolize females, and age- or condition-dependent models of female choice. We used 18 years of genetic and demographic data to examine the mating system and patterns of multiple paternity in a free-living population of golden-mantled ground squirrels (Callospermophilus lateralis). The mating system was polygynandrous, but opportunity for sexual selection was lower for females than for males. Annual reproductive success of males was low for yearlings and new immigrants and increased with breeding tenure in the population. Multiple paternity was evident in 62% of litters. In accordance with the socioecological model of male monopolization, rates of multiple paternity decreased with female spatial clustering, unless male–male competition, as indicated by male density, was also high. From Bateman gradients, we found no direct fitness benefit of multiple paternity for females. Though not statistically significant, multiple paternity appeared to decrease with maternal age and peri-oestrous mass, in possible support of the female choice model. Together, our results suggest that variation in the rate of multiple paternity in golden-mantled ground squirrels was determined by density and the active strategies of males and females.Significance statementSince the advent of molecular parentage assignment several decades ago, we have known that females of many species produce offspring with different fathers. Several theories have been developed for why females produce multiply-sired clutches or litters, but rarely are we able to identify the environmental, social, or individual conditions under which they do so. In this study, we genotyped offspring produced in one population of ground squirrels over 18 years, and found that the frequency of multiple paternity varied considerably from year to year, that density of female kin interacted with male density to influence multiple paternity, and that older and heavier females tended to be less likely to produce multiply-sired litters. These results demonstrate how dynamic population and individual characteristics of breeding males and females contribute to mating system variation in the same population over time

Polyandry and Polygyny in a Social Rodent: An Integrative Perspective Based on Social Organization, Copulations, and Genetics

“…A single year of observations of copulations and genetic assignments of paternity would have given a misleading impression of the overall frequencies of behavioral and genetic estimates of polyandry and polygyny for WTPDs. Several other studies have documented large annual variation in the frequencies of behavioral and genetic polyandry and polygyny as reported here for WTPDs (e.g., Schwagmeyer and Brown, 1983;Moller, 1992, 1998;Hare et al, 2004;Isvaran and Clutton-Brock, 2006;Bergeron et al, 2011;Wells et al, 2017). Possible reasons for so much annual variation include yearly differences in factors such as weather (Bergeron et al, 2011;Martin et al, 2014), density of females (Emlen and Oring, 1977;Wells et al, 2017), female age and female body mass (Cotton et al, 2006;Jones et al, 2012;Hoogland, 2013b), reproductive synchrony among females (Emlen and Oring, 1977;Hoogland, 2007), and the operational sex ratio (i.e., ratio of the number of sexually mature females ready to copulate to the number of sexually mature males ready to copulate; Emlen and Oring, 1977;Michener and McLean, 1996).…”

“…Information from WTPD social organization, for example, helped us to know which males were likely to copulate with an estrous female, and information from both social organization and copulations helped us to know which males to consider as possible candidate sires for each offspring. Our research was an extension of previous research on other species of ground-dwelling squirrels (e.g., Hanken and Sherman, 1981;Lacey et al, 1997;Goossens et al, 1998;Raveh et al, 2011;Wells et al, 2017), and should be informative for other social species as well. Our results underscore the valuable insights that can result from integrating diverse perspectives on the mating system gathered from long-term behavioral and genetic studies of natural populations.…”

Litter relocation behavior in two species of ground‐dwelling squirrels

“…We also summarized conspecific interactions associated with litter moves to explore the potential role of the social environment. Female relatedness was calculated from pedigrees based on mother–pup and littermate relations (Armitage & Johns, ; Wells et al, ).…”

Developmental and social constraints on early reproduction in an asocial ground squirrel

“…were categorized as female relatives; females present in the same locality but not part of the same matriline pedigree were categorized as unrelated (Wells & Van Vuren, ). Because some male golden‐mantled ground squirrels mate with multiple females (Wells et al ., ), it is possible that yearling females may also be in the presence of female kin related through the paternal line. To assess this possibility, we used the program ML‐Relate (Kalinowski, Wagner & Taper, ) to estimate pairwise relatedness from female multilocus genotypes in a subset of years (2008–2015, Wells et al ., ).…”

“…Because some male golden‐mantled ground squirrels mate with multiple females (Wells et al ., ), it is possible that yearling females may also be in the presence of female kin related through the paternal line. To assess this possibility, we used the program ML‐Relate (Kalinowski, Wagner & Taper, ) to estimate pairwise relatedness from female multilocus genotypes in a subset of years (2008–2015, Wells et al ., ). Estimates of genetic relatedness confirmed most unrelated pairs (17/20 r = 0), but 3/20 ‘unrelated’ pairs appeared related at r = 0.09–0.13, equivalent to the level of third‐order relatives.…”