Abstract

Cryptic female choice may enable polyandrous females to avoid inbreeding or bias offspring variability at key loci after mating. However, the role of these genetic benefits in cryptic female choice remains poorly understood. Female red junglefowl, Gallus gallus, bias sperm use in favour of unrelated males. Here, we experimentally investigate whether this bias is driven by relatedness per se, or by similarity at the major histocompatibility complex (MHC), genes central to vertebrate acquired immunity, where polymorphism is critical to an individual's ability to combat pathogens. Through experimentally controlled natural matings, we confirm that selection against related males' sperm occurs within the female reproductive tract but demonstrate that this is more accurately predicted by MHC similarity: controlling for relatedness per se, more sperm reached the eggs when partners were MHC-dissimilar. Importantly, this effect appeared largely owing to similarity at a single MHC locus (class I minor). Further, the effect of MHC similarity was lost following artificial insemination, suggesting that male phenotypic cues might be required for females to select sperm differentially. These results indicate that postmating mechanisms that reduce inbreeding may do so as a consequence of more specific strategies of cryptic female choice promoting MHC diversity in offspring.

Highlights

  • Offspring of genetically similar parents often suffer reduced fitness, either as a result of inbreeding depression [1,2] or reduced genetic variation at specific loci [3]

  • Further investigating the relative role of genetic relatedness per se and major histocompatibility complex (MHC) similarity, we found that models including similarity at MHC class I minor, and MHC class I minor together with genetic relatedness, were a much better explanation of the data than models including relatedness rspb.royalsocietypublishing.org Proc R Soc B 280: 20131296

  • We found no evidence that failure to transfer and/or store sperm was predicted by relatedness or MHC similarity

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Summary

Introduction

Offspring of genetically similar parents often suffer reduced fitness, either as a result of inbreeding depression [1,2] or reduced genetic variation at specific loci [3]. MHC class I genes are associated primarily with intracellular pathogens, whereas MHC class II genes interact with extracellular pathogens [6] Reduced diversity at these MHC loci can compromise an individual’s ability to combat pathogens [7,8,9,10], and females should select partners to optimize the genetic diversity of their offspring [9,10,11,12,13]. Cryptic female choice might allow optimization of offspring MHC by biasing sperm use in response to the females’ MHC similarity to a male [12,18,19,20,21]. This hypothesis remains little explored and empirically unresolved. Consistent with general expectations, some studies have found evidence of fertilization bias promoting the MHC heterozygosity of

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