Paternity in wild ring‐tailed lemurs (Lemur catta): Implications for male mating strategies

Abstract

In group‐living species with male dominance hierarchies where receptive periods of females do not overlap, high male reproductive skew would be predicted. However, the existence of female multiple mating and alternative male mating strategies can call into question single‐male monopolization of paternity in groups. Ring‐tailed lemurs (Lemur catta) are seasonally breeding primates that live in multi‐male, multi‐female groups. Although established groups show male dominance hierarchies, male dominance relationships can break down during mating periods. In addition, females are the dominant sex and mate with multiple males during estrus, including group residents, and extra‐group males—posing the question of whether there is high or low male paternity skew in groups. In this study, we analyzed paternity in a population of wild L. catta from the Bezà Mahafaly Special Reserve in southwestern Madagascar. Paternity was determined with 80–95% confidence for 39 offspring born to nine different groups. We calculated male reproductive skew indices for six groups, and our results showed a range of values corresponding to both high and low reproductive skew. Between 21% and 33% of offspring (3 of 14 or three of nine, counting paternity assignments at the 80% or 95% confidence levels, respectively) were sired by extra‐troop males. Males siring offspring within the same group during the same year appear to be unrelated. Our study provides evidence of varying male reproductive skew in different L. catta groups. A single male may monopolize paternity across one or more years, while in other groups, >1 male can sire offspring within the same group, even within a single year. Extra‐group mating is a viable strategy that can result in extra‐group paternity for L. catta males.

Heteropaternity of twins in ring‐tailed lemurs (Lemur catta)

“…Other L. catta colonies show similarly high multiple‐offspring birth rates that range between 18 and 54% (Drea, ; Pasztor & Van Horn, ; St Clair et al, ) due to food abundance in captivity. Wild L. catta in nonprovisioned populations show lower rates of twinning/triplets, with multiple‐offspring births occurring only rarely (Bezá Mahafaly Special Reserve: Pastorini et al, ; Parga et al, ; Gould, personal communication; Anja Reserve: L. Gould, personal communication Aug. 9, 2018). Even wild L. catta in areas with a history of tourist provisioning—for example, Berenty Reserve—only have a twinning rate of 2% (Jolly et al, ; Koyama et al, ).…”

“…In other nonhuman primates, dizygotic twinning is more common than monozygotic twinning (callitrichids: Digby, Ferrari, & Saltzman, ; macaques: Sugiyama et al, ; mouse lemurs: Radespiel et al, ), which is also the case among most human populations (Hall, ; Hoekstra et al, ; Tong, Caddy, & Short, ). Previous research has documented monozygotic twins among wild L. catta in Bezá Mahafaly Special Reserve, Madagascar via DNA analysis (Parga et al, ; Pastorini et al, ). It is unclear why none of the infant pairs on SCI were monozygous, but this finding may have been a consequence of the small sample size of twins evaluated in our study.…”

“…Our study investigated twinning and heteropaternity in a provisioned non‐wild population of the ring‐tailed lemur ( L. catta ), a seasonally breeding strepsirhine endemic to southwestern, south‐central, and the southernmost regions of Madagascar (Gould & Sauther, ; Jolly, ; Sauther, Sussman, & Gould, ). Monozygotic twins have been opportunistically discovered in wild L. catta as part of genetic analyses conducted for other studies (Parga et al, ; Pastorini et al, ), and dizygotic twins have been observed in the wild (Koyama et al, ) and in captivity (Drea, ; Pasztor & Van Horn, ) by noting twin pairs of different sexes. Although no study has used genetic data to evaluate the relative proportion of monozygotic versus dizygotic twinning in this species, data from most captive L. catta colonies show a higher proportion (>50%) of opposite‐sexed rather than same‐sexed twins (Pasztor & Van Horn, ; Drea, ; but see St Clair, Campbell‐Palmer, & Lathe, ).…”

“…A relationship between twinning incidence and food availability exists in L. catta . In the wild under conditions of relatively low food availability, twinning is rare but occasionally occurs (Bezá Mahafaly Special Reserve: Parga et al, ; Pastorini et al, ; L. Gould, personal communication). Twinning has also been observed among wild L. catta in nonprovisioned but especially resource‐rich areas such as Anja Reserve (L. Gould, personal communication Aug. 9, 2018), where lemurs have access to abundant natural food and water year‐round (Gould & Gabriel, ), as well as in areas of tourist provisioning (i.e., Berenty: Jolly et al, ; Koyama et al, ).…”

“…Female sexual preference for novel males has been noted in captivity (Pereira & Weiss, ). Genetic paternity analyses on one wild L. catta population have revealed that extra‐group males sired between 21 and 33% of offspring (Parga et al, ). However, no study has performed a genetic evaluation of twins in this species to assess the relative proportion of mono versus dizygotic twins, and no study has evaluated genetic data on twins to confirm heteropaternity in this species.…”