The effects of male philopatry on reproductive behaviors and fitness in Columbian ground squirrels (Urocitellus columbianus)

Abstract

Decreased fitness is a consequence of inbreeding in many species. As a result, a variety of behavioral mechanisms, such as dispersal, are employed be mammals to avoid mating with relatives. Columbian ground squirrels (Urocitellus columbianus) are a polygynandrous species in which females remain philopatric, and males have a mixed dispersal pattern, with some males emigrating and others remaining philopatric residents. The goals of this study were to determine the effects of the presence of close female kin (mothers and littermate sisters) on the mating habits of Columbian ground squirrels, explain the mixed dispersal pattern in males, and to determine whether inbreeding occurs in this species. We additionally compared the fitness (measured as number of mating partners and offspring produced) and several other variables (mass, hibernation emergence date, age, and length of time living in the population) of males to detect whether residency status (immigrant males compared to philopatric resident males) influences male fitness, and, if so, what variables are related to the difference. We addressed these goals using a longitudinal dataset of the reproductive behaviors of a population of Columbian ground squirrels in Sheep River Provincial Park, Alberta, Canada. Our analysis included data from 2005-2015 and had a total sample of 56 individual adult males and 90 individual adult females. Some individuals lived in the population multiple years, resulting in 127 samples of males and 244 samples of females (191 of which had logs of mating partners). Through our analysis, we found that the presence of close female relatives resulted in decreased male mating likelihood; male samples that did not co-occur with their mother were 1.34 times more likely to mate with one or more females, and male samples that did not co-occur with littermate sister(s) were 1.45 times more likely to mate. The data supports that the decreased mating likelihood may be a result of age. In addition, although male samples and female samples co-occurred equally with their mothers, females were 1.86 times more likely to co-occur with another littermate sister. We suggest that this may be a result of sex-biased aggression from mothers towards sons. In regards to inbreeding, pairs of a non-related male and females (i.e. not mother-son or brother-littermate sister) mated 8.83 times more often than related pairs (mother-son and brother-littermate sister), and only one instance of inbreeding between a male and close female relative (mother) were detected during the study. Thus, inbreeding is avoided in this species, potentially through a combination of dispersal and recognition of relatives. By comparing resident male samples and immigrant male samples, we found that resident male samples were 1.28 times more likely to mate than immigrant male samples, and resident male samples had significantly more mating partners on average (7.4±5.1 SD mates compared to 4.7±5.1 SD mates; p=0.008). We concluded that this was the result of the effects of age and emergence date differences between resident male and immigrant male samples. Interestingly, despite more mating partners, there was no significant difference in the average number of offspring produced by resident and immigrant male samples (6.1±6.0 SD offspring and 5.0±6.8 SD offspring; p=0.348). We suggest that this may be a result of inbreeding depression from moderate inbreeding of distant relatives mating. Immigrant male samples had a nearly significant trend of producing more offspring per mate compared to resident male samples (interaction between residency status and number of mates in regards to number of offspring produced: p=0.092). For adult male resident samples, for every one mate increase there was a 0.9 offspring increase in number of offspring produced (r2=0.50, p<0.001), but for adult immigrant male samples, for every one mate increase there was a 1.1 offspring increase in number of offspring produced (r2=0.69, p<0.001).