The evolution of a rare mammalian trait - benefits and costs of male philopatry in proboscis bats

Abstract

While inbreeding avoidance is widely accepted as the major driver of female natal dispersal, the evolution of male philopatry is still poorly understood and discussed to be driven by male mating strategy, mate competition among male kin and kin cooperation. During a twelve-year study, we gathered detailed genetic and observational data of individually marked proboscis bats to assess the degree of male philopatry as well as its costs and benefits to improve the understanding of its evolution. Our results reveal several patrilines with simultaneous presence of closely related males and a small proportion of unrelated immigrant males in their colonies. Philopatric males benefit from avoiding the costs of immigration into foreign colonies through significantly longer tenure, better integration (i.e. frequent nocturnal presence in the colonies) and consequently significantly higher reproductive success compared to immigrant males. Finally, we illustrate that despite a high proportion of philopatric males in the groups, the number of closely related competing males is low. Thus, the hypothesised costs of mate competition among male kin seem to be low in promiscuous mammalian societies with unrelated females and a small degree of male immigration and are readily outweighed by the benefits of staying in the natal group.

Figure 1

The age of disappearance from the natal colony C5 of female and male colony offspring. All female offspring dispersed prior to reproduction. Individuals with information on birth date and disappearance time born between 2008 and 2014 are shown. The observation of these individuals ended in November 2016. Please note the logarithmic scale of the y-axis.

Figure 2

Patrilines of the three study colonies Cabina 5 (C5), Riverstation (RS) and Casa Grande (CG). All present adult males and – if assigned – their male ancestors present prior to 2011 are shown. Each column represents an individual male. Grey columns indicate the male’s presence. Solid lines indicate a father-son relationship and dashed lines beneath columns indicate males sharing the same mother. Philopatric males are marked with ‘★’, immigrants with ‘i’ and males with unknown dispersal status with ‘?’. If a male was caught as juvenile between 2011 and 2015, the year of birth is indicated with a white star in the respective columns. Please note that two philopatric adult males transferred permanently from C5 to RS, thus are listed in both colonies. The direction of one father-son relationship in RS could not be solved (marked with a two-sided arrow).

Figure 3

Minimum individual tenure of philopatric and immigrant males. Males caught between 2005 and 2014 are included. The observation of these individuals ended in October 2015 (RS), July 2016 (CG) and November 2016 (C5). The difference is statistically significant with p < 0.001. Please note that two philopatric adult males transferred permanently from C5 to RS, thus are included in the calculations with their tenure as philopatric and with their tenure as immigrant males.

Figure 4

Size comparison of philopatric and immigrant males. Length of forearm, third and fifth finger of adult philopatrics (C5: n = 15, RS: n = 3, CG: n = 10) and adult immigrants (C5: n = 7, RS: n = 2) is shown. All measurements were performed by the same person (L.G) at a minimum age of one year, when all bats were fully-grown. All differences are statistically significant with p < 0.001.

Figure 5

Mean number of sired offspring per mating period by philopatric and immigrant males. Offspring of fathers with known dispersal status from six different mating periods between 2010 and 2014 are included (n = 45 offspring). The number of sired offspring by each male is averaged for the six mating periods the males were present as adult individuals. The difference is statistically significant with p = 0.029.

Figure 6

The proportion of relatedness classes of adult male dyads present within the same group and their direct competition. Both mating periods in 2013 and 2014 are shown [‘postpartum oestrous mating period’ (PEMP) and ‘seasonal mating period’ (SMP)]. The first bar (‘Simultaneous presence’) reflects the proportion of relatedness classes of male pairs that were simultaneously present in the same social group. The second bar (‘Agonistic interaction’) shows the proportion of relatedness classes of all agonistic interactions and the involved male pairs. The third bar (‘Same mate copulation/copulation attempt’) shows the proportion of relatedness classes of male pairs that copulated or attempted to copulate with the same female during the same mating period. The sample size of male pairs in each category and mating period is shown.