Mating strategies and genetic constitution in the gray mouse lemur (Microcebus murinus) in Kirindy Forest, Madagaskar
Final Report Abstract
Understanding female promiscuity poses a major problem in the study of animal behaviour. Females, in contrast to males, cannot increase their number of offspring by mating with multiple partners during one ovarian cycle – they only have a few ova. In addition, mating is usually risky for females: they can catch sexually transmitted diseases and are often harmed by toxic male fluids or spiny penises. Yet, natural observations over a range of species have revealed that female promiscuity is extremely common, and this is especially true in mammals. So why do females mate with multiple partners? In some invertebrates, the answer is straightforward: males convince females to mate by offering them food gifts. Elsewhere, males can take advantage of their strength to force females. Rape, although rare in nature, occurs in some species such as orangutans or dolphins. Another classical hypothesis relies on the observation that males frequently kill unrelated offspring. This may encourage females to mate with multiple partners to dilute paternity. Finally, females may mate promiscuously to obtain good genes for their offspring, by selecting sperm through hidden post-copulatory processes occurring in the genital tract. In grey mouse lemurs (Microcebus murinus), a small nocturnal primate from Madagascar, males do not provide food gifts, while infanticide is unlikely to represent a major threat. Yet, females can mate with up to 15 males when they are sexually receptive, once a year. We tested the two remaining hypotheses regarding the evolution of polyandry. First, females may mate with multiple males to decrease the costs of sexual harassment. We designed experiments in a captive population to test this hypothesis. We manipulated the size of the females by an increase or reduction of the food supply in such a way that in one experimental approach the females were larger than males and smaller in the other group. While the larger females were expected to mate with fewer males because they would be better able to defend themselves against undesired overtures, they had more sexual partners than the smaller ones. These results suggest that polyandry represents an active strategy which may provide benefits to females. As a logical next step, we tested whether females may seek multiple partners to select sperm carrying good or compatible genes. We examined patterns of parentage in wild grey mouse lemurs living in western Madagascar in relation to genes of the major histocompatibility complex (MHC). MHC genes play a key role in the immune system by recognizing pathogens. It may be advantageous for females to select sperm carrying dissimilar MHC genotypes to their own, because this would increase offspring MHC diversity, thereby allowing them to recognize and fight more pathogens. We used parent-offspring triads to test whether MHC heterozygous fathers, whose gametes can carry one or the other MHC allele, preferentially transmit the allele, which is most dissimilar to the allele carried by the maternal gamete. Fertilization appears random with respect to MHC for male, but not for female offspring. There, paternal alleles that are most similar to maternal ones are transmitted more often. This result is intriguing, and may be understood if mothers adjust their reproductive strategies to the sex of their future offspring. When there is no inbreeding risk – as in our study population - choice for MHC similarity might allow mothers that have reproduced successfully, and thus likely carry MHC genes that are well-adapted to their environment, to select good paternal genes. But parasite communities vary spatially, and only daughters live in the same environment as their mothers. In contrast, males typically emigrate before sexual maturity. As a result, choice for MHC similarity might only be advantageous for daughters not sons. To conclude, these findings suggest that female grey mouse lemurs actively seek matings from multiple males, and that this may allow them to bias fertilization chances towards sperm carrying adaptive MHC genotypes for their future offspring.
Publications
- The hidden benefits of sex: Evidence for MHC associated mate choice in primate societies. BioEssays 32: 940-948, 2010
Setchell, J. M. and Huchard, E.
- Convenience polyandry or convenience polygyny? Costly sex under female control in a promiscuous primate. Proceeding of the Royal society of London B 279: 1371-1379, 2012
Huchard, E., Canale, C. I., Le Gros, C., Perret, M., Henry, P.-Y., and Kappeler, P. M.
- Mutual mate choice in a femaledominant and sexually dimorphic primate. American Journal of Physical Anthropology 147: 370-9, 2012
Gomez, D., Huchard, E., Henry, P.-Y., and Perret, M.
(See online at https://doi.org/10.1002/ajpa.21653)
