Abstract

Within-population variation in the traits underpinning reproductive output has long been of central interest to biologists. Since they are strongly linked to lifetime reproductive success, these traits are expected to be subject to strong selection and, if heritable, to evolve. Despite the formation of durable pair bonds in many animal taxa, reproductive traits are often regarded as female-specific, and estimates of quantitative genetic variation seldom consider a potential role for heritable male effects. Yet reliable estimates of such social genetic effects are important since they influence the amount of heritable variation available to selection. Based on a 52-year study of a nestbox-breeding great tit (Parus major) population, we apply "extended" bivariate animal models in which the heritable effects of both sexes are modeled to assess the extent to which males contribute to heritable variation in seasonal reproductive timing (egg laying date) and clutch size, while accommodating the covariance between the two traits. Our analyses show that reproductive timing is a jointly expressed trait in this species, with (positively covarying) heritable variation for laydate being expressed in both members of a breeding pair, such that the total heritable variance is 50% larger than estimated by traditional models. This result was robust to explicit consideration of a potential male-biased environmental confound arising through sexually dimorphic dispersal. In contrast to laydate, males' contribution to heritable variation in clutch size was limited. Our study thus highlights the contrasting extent of social determination for two major components of annual reproductive success, and emphasizes the need to consider the social context of what are often considered individual-level traits.

Highlights

  • The classic perspective of quantitative genetics is that an individual’s phenotype is determined by its genotype (G), its environmental experiences (E), and any interactions between the two (i.e., P = G + E + G × E)

  • While the presence of spatial autocorrelation was strongly supported, this model indicated that spatial autocorrelation does not account for the heritable male effects on reproductive timing we report, since the additive geneticvariance estimates for laydate from this third model closely matched those of the preceding model (Table 1)

  • We used a 52-year study of great tit breeding behavior to assess whether males contribute to heritable variation in laydate and clutch size, finding support for heritable male effects on laydate

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Summary

Introduction

A quantitative genetic approach—and, in particular, the animal model (Henderson 1953, 1975)—is able to infer the heritable component of individual heterogeneity by leveraging the (partial) genotypic replication inherent in sampling known relatives In another passerine bird, the song sparrow (Melospiza melodia), a heritable contribution of male heterogeneity to variation in reproductive timing has been described, and a positive covariance of the male and female genetic effects means the estimated total heritable variance in laydate is doubled once the contribution via males is explicitly considered (Germain et al 2016). Whether male genetic effects extend to reproductive quantum (i.e., clutch or litter size), the other principal axis of within-population variation in reproductive output, has been more neglected still (though see: van Noordwijk et al 1980; Gibbs 1988; van der Jeugd and McCleery 2002; van Noordwijk et al 1981a), despite being linked to both reproductive timing and lifetime reproductive success in many avian study populations (Klomp 1970)

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