Mate choice for major histocompatibility complex complementarity in a strictly monogamous bird, the grey partridge (Perdix perdix)

Abstract

BackgroundSexual selection has been hypothesised as favouring mate choice resulting in production of viable offspring with genotypes providing high pathogen resistance. Specific pathogen recognition is mediated by genes of the major histocompatibility complex (MHC) encoding proteins fundamental for adaptive immune response in jawed vertebrates. MHC genes may also play a role in odour-based individual recognition and mate choice, aimed at avoiding inbreeding. MHC genes are known to be involved in mate choice in a number of species, with ‘good genes’ (absolute criteria) and ‘complementary genes’ (self-referential criteria) being used to explain MHC-based mating. Here, we focus on the effect of morphological traits and variation and genetic similarity between individuals in MHC class IIB (MHCIIB) exon 2 on mating in a free-living population of a monogamous bird, the grey partridge.ResultsWe found no evidence for absolute mate choice criteria as regards grey partridge MHCIIB genotypes, i.e., number and occurrence of amino acid variants, though red chroma of the spot behind eyes was positively associated with male pairing success. On the other hand, mate choice at MHCIIB was based on relative criteria as females preferentially paired with more dissimilar males having a lower number of shared amino acid variants. This observation supports the ‘inbreeding avoidance’ and ‘complementary genes’ hypotheses.ConclusionsOur study provides one of the first pieces of evidence for MHC-based mate choice for genetic complementarity in a strictly monogamous bird. The statistical approach employed can be recommended for testing mating preferences in cases where availability of potential mates (recorded with an appropriate method such as radio-tracking) shows considerable temporal variation. Additional genetic analyses using neutral markers may detect whether MHC-based mate choice for complementarity emerges as a by-product of general inbreeding avoidance in grey partridges.Electronic supplementary materialThe online version of this article (doi:10.1186/s12983-017-0194-0) contains supplementary material, which is available to authorized users.

Darwin, sexual selection, and the brain

“…Somewhat related to the "good genes" hypothesis is selection for complementary genes, which motivates preferences for conspecifics over heterospecifics and might also be important in mate choice within populations when it comes to certain genes such as the major histocompatibility complex (37). A favorite hypothesis of theoretical population geneticists is Fisherian runaway sexual selection, but its empirical support, usually based on demonstrating genetic correlations of traits and preferences, is somewhat sparse (38).…”

Sperm is a sexual ornament in rose bitterling

“…The proximate mechanism by which individuals judge MHC dissimilarity in mating partners has been persuasively demonstrated to be through olfactory cues in a range of vertebrates (Eggert et al ., ; Penn, ; Ziegler et al ., ), even including taxa, such as birds, with relatively poorly‐developed olfaction (e.g. Rymešová et al ., ). The functional benefits of selecting a mate with dissimilar MHC variants are recognized as coming through increased MHC diversity and elevated heterozygosity in the offspring, as well as from an enhanced performance accruing from specific haplotype combinations (Tregenza & Wedell, ).…”

Kin grouping is insufficient to explain the inclusive fitness gains of conspecific brood parasitism in the common eider

“…In the absence of support for the “nest site fidelity” model, we suggest that the “kin recognition” model is the preferred mechanism that allows brood parasitism to persist (Andersson, , ). Two hypothesized modes of kin recognition in avian species are visual and olfactory (Andersson et al, ; Rymesova et al, ). Andersson et al () used camera monitoring and found interactions between host and parasitizer were “tolerant” between related individuals.…”

“…The second form of kin recognition, which has received little attention relative to brood parasitism, is olfactory stimulus. Historically, few avian species were thought to have any useful form of olfactory senses, but recent work has provided a new perspective on a broader range of avian taxa in this regard (Caro, Balthazart, & Bonadonna, ; Leclaire, Bourret, & Bonadonna, ; Rymesova et al, ). In birds, the uropygial gland in particular is believed to secrete preening oils with chemical signals unique to that individual, which is available for detection by others through olfaction (Mardon, Saunders, & Bonadonna, ).…”

“…For the final element of conspecific brood parasitism (relatedness), we can hypothesize two mechanisms that would maintain high levels of genetic relatedness between host and parasitizer: “kin recognition plus kin preference” or “philopatry plus nest site fidelity.” The “kin recognition” model does not necessarily require philopatry or nest site fidelity, and instead relies on either parasitizers seeking out, recognizing and preferentially parasitizing kin, or for hosts to recognize and preferentially accept eggs from kin (Lopez‐Sepulcre and Kokko (). In birds this could be the result of visual and olfactory cues to discriminate between kin and nonkin in proximity to the host's nest or potentially even similarity of egg patterns to the host's eggs (Andersson, Waldeck, Hanssen, & Moe, ; Rymesova et al, ). The “nest site fidelity” model does not necessarily require either kin recognition or kin preference, but is instead simply an artefact of (a) philopatry (the tendency for a female to nest in the general area from which she hatched), (b) nest site fidelity (the tendency for a female to nest near her previous year's nesting site), and (c) local parasitism (females parasitizing nearby nests).…”