<scp>MHC</scp>‐disassortative mate choice and inbreeding avoidance in a solitary primate

Huchard, Élise; Baniel, Alice; Schliehe-Diecks, Susanne; Kappeler, Peter M.

doi:10.1111/mec.12349

Cited by 53 publications

(58 citation statements)

References 79 publications

(121 reference statements)

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“…Choosing partners with maximal or optimal genetic dissimilarity may help to avoid inbreeding or excessive outbreeding, respectively. To increase offspring diversity at key functional loci in a natural population, a recent study indicated that inbreeding avoidance was along with disassortative mate choice at DRB , but not at DQB locus [45]. Our results also seem to support this point.…”

Section: Discussionsupporting

confidence: 83%

Genetic diversity and differentiation of the rhesus macaque (Macaca mulatta) population in western Sichuan, China, based on the second exon of the major histocompatibility complex class II DQB (MhcMamu-DQB1) alleles

Yao

Dai

et al. 2014

BMC Evol Biol

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AbstractsBackgroundRhesus macaques living in western Sichuan, China, have been separated into several isolated populations due to habitat fragmentation. Previous studies based on the neutral or nearly neutral markers (mitochondrial DNA or microsatellites) showed high levels of genetic diversity and moderate genetic differentiation in the Sichuan rhesus macaques. Variation at the major histocompatibility complex (MHC) loci is widely accepted as being maintained by balancing selection, even with a low level of neutral variability in some species. However, in small and isolated or bottlenecked populations, balancing selection may be overwhelmed by genetic drift. To estimate microevolutionary forces acting on the isolated rhesus macaque populations, we examined genetic variation at Mhc-DQB1 loci in 119 wild rhesus macaques from five geographically isolated populations in western Sichuan, China, and compared the levels of MHC variation and differentiation among populations with that previously observed at neutral microsatellite markers.Results23 Mamu-DQB1 alleles were identified in 119 rhesus macaques in western Sichuan, China. These macaques exhibited relatively high levels of genetic diversity at Mamu-DQB1. The Hanyuan population presented the highest genetic variation, whereas the Heishui population was the lowest. Analysis of molecular variance (AMOVA) and pairwise FST values showed moderate genetic differentiation occurring among the five populations at the Mhc-DQB1 locus. Non-synonymous substitutions occurred at a higher frequency than synonymous substitutions in the peptide binding region. Levels of MHC variation within rhesus macaque populations are concordant with microsatellite variation. On the phylogenetic tree for the rhesus and crab-eating macaques, extensive allele or allelic lineage sharing is observed betweenthe two species.ConclusionsPhylogenetic analyses confirm the apparent trans-species model of evolution of the Mhc-DQB1 genes in these macaques. Balancing selection plays an important role in sharing allelic lineages between species, but genetic drift may share balancing selection dominance to maintain MHC diversity. Great divergence at neutral or adaptive markers showed that moderate genetic differentiation had occurred in rhesus macaque populations in western Sichuan, China, due to the habitat fragmentation caused by long-term geographic barriers and human activity. The Heishui population should be paid more attention for its lowest level of genetic diversity and relatively great divergence from others.

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Section: Discussionsupporting

confidence: 83%

Genetic diversity and differentiation of the rhesus macaque (Macaca mulatta) population in western Sichuan, China, based on the second exon of the major histocompatibility complex class II DQB (MhcMamu-DQB1) alleles

Yao

Dai

et al. 2014

BMC Evol Biol

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“…5,89,96,99,134,137 Additionally, this relationship has been detected solely as female preference for males. Similar findings were detected by Kamiya et al Sauermann et al 137 Huchard et al 135 Huchard et al 135 Yang et al 139 Huchard et al 90 Setchell et al 89 Schwensow et al 5 …”

Section: Selection For Mates With Greater Mhc Diversitysupporting

confidence: 78%

“…Sauermann et al 137 Sauermann et al 137 Huchard et al 135 Yang 90 Setchell et al 89 Schwensow et al 5 Schwensow et al 5 Sauermann et al 137…”

Section: Mate Choice Preference Mate Choice Preferenceunclassified

“…66 Nonhuman primate studies in the wild, obligated to rely on neutral markers for parentage assignment, have usefully incorporated both neutral and MHC relatedness to reveal significant relative importance of the MHC in mate selection. 89,90 Related to the problem of linkage between MHC and genome-wide diversity within individuals is the complication of population structure. MHC allele frequencies vary across ethnic groups and populations, 91,92 and selfpreference of subpopulations is characterized by distinctive frequencies of alleles.…”

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confidence: 99%

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Examining the evidence for major histocompatibility complex-dependent mate selection in humans and nonhuman primates

Winternitz¹,

Abbate²

2015

RRB

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Compounds of the major histocompatibility complex (MHC) are integral for effective vertebrate adaptive immune response, and are also implicated as cues for sexual selection. The evidence for this is supportive of MHC-based preference for diverse and dissimilar mating partners, in a range of vertebrates from fish to nonhuman primates. However, the evidence for a similar role of these genes and the evolutionary benefits of their diversity in human mate choice has been more controversial. Here, we review the results of 34 primary studies on MHC-mediated mate choice in humans and nonhuman primates in an effort to understand what processes may underscore, or belie, such differences. Both human and nonhuman primate studies show evidence of mate selection for MHC-dissimilarity and diversity, with fewer results in support of mate selection for optimal diversity or for specific "good gene". In general, stronger support comes from female-choice studies as opposed to male-choice studies (though male preferences and choice are investigated less often). This review suggests that the majority of mate choice results from contemporary human studies are consistent with our evolutionary history, but also reveals that only in humans do we find evidence for preference for mates with similar MHC composition. Overall, we show that contextual nuances, namely, population structure, multiple sensory cues that signal different information, and hormonal influences may explain the conflicting results observed for the role of MHC in human sexual preference, and argue for the exploration of such caveats in less well-studied systems to discern between general patterns and qualities unique to humans.

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“…In support of this assumption, a possible link between highly divergent or specific MHC genotypes and individual fitness (Schad et al 2005; Schwensow et al 2007, 2010a, b; Sommer et al 2014) and mate choice (Schwensow et al 2008a, b; Huchard et al 2013) has been suggested for two widely distributed lemurs— Microcebus murinus and Cheirogaleus medius (Cheirogaleidae, Primates). Consequently, the evaluation of MHC variation retained in populations of endangered confamiliar species can provide valuable insights to assess their viability.…”

Section: Introductionmentioning

confidence: 97%

MHC class II variation in a rare and ecological specialist mouse lemur reveals lower allelic richness and contrasting selection patterns compared to a generalist and widespread sympatric congener

et al. 2015

Self Cite

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The polymorphism of immunogenes of the major histocompatibility complex (MHC) is thought to influence the functional plasticity of immune responses and, consequently, the fitness of populations facing heterogeneous pathogenic pressures. Here, we evaluated MHC variation (allelic richness and divergence) and patterns of selection acting on the two highly polymorphic MHC class II loci (DRB and DQB) in the endangered primate Madame Berthe’s mouse lemur (Microcebus berthae). Using 454 pyrosequencing, we examined MHC variation in a total of 100 individuals sampled over 9 years in Kirindy Forest, Western Madagascar, and compared our findings with data obtained previously for its sympatric congener, the grey mouse lemur (Microcebus murinus). These species exhibit a contrasting ecology and demography that were expected to affect MHC variation and molecular signatures of selection. We found a lower allelic richness concordant with its low population density, but a similar level of allelic divergence and signals of historical selection in the rare feeding specialist M. berthae compared to the widespread generalist M. murinus. These findings suggest that demographic factors may exert a stronger influence than pathogen-driven selection on current levels of allelic richness in M. berthae. Despite a high sequence similarity between the two congeners, contrasting selection patterns detected at DQB suggest its potential functional divergence. This study represents a first step toward unravelling factors influencing the adaptive divergence of MHC genes between closely related but ecologically differentiated sympatric lemurs and opens new questions regarding potential functional discrepancy that would explain contrasting selection patterns detected at DQB.Electronic supplementary materialThe online version of this article (doi:10.1007/s00251-015-0827-4) contains supplementary material, which is available to authorized users.

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MHC‐disassortative mate choice and inbreeding avoidance in a solitary primate

Cited by 53 publications

References 79 publications

Genetic diversity and differentiation of the rhesus macaque (Macaca mulatta) population in western Sichuan, China, based on the second exon of the major histocompatibility complex class II DQB (MhcMamu-DQB1) alleles

Genetic diversity and differentiation of the rhesus macaque (Macaca mulatta) population in western Sichuan, China, based on the second exon of the major histocompatibility complex class II DQB (MhcMamu-DQB1) alleles

Examining the evidence for major histocompatibility complex-dependent mate selection in humans and nonhuman primates

MHC class II variation in a rare and ecological specialist mouse lemur reveals lower allelic richness and contrasting selection patterns compared to a generalist and widespread sympatric congener

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