Sex‐specific additive genetic variances and correlations for fitness in a song sparrow (Melospiza melodia) population subject to natural immigration and inbreeding

Abstract

Quantifying sex-specific additive genetic variance (V ) in fitness, and the cross-sex genetic correlation (r ), is prerequisite to predicting evolutionary dynamics and the magnitude of sexual conflict. Further, quantifying V and r in underlying fitness components, and genetic consequences of immigration and resulting gene flow, is required to identify mechanisms that maintain V in fitness. However, these key parameters have rarely been estimated in wild populations experiencing natural environmental variation and immigration. We used comprehensive pedigree and life-history data from song sparrows (Melospiza melodia) to estimate V and r in sex-specific fitness and underlying fitness components, and to estimate additive genetic effects of immigrants alongside inbreeding depression. We found evidence of substantial V in female and male fitness, with a moderate positive cross-sex r . There was also substantial V in male but not female adult reproductive success, and moderate V in juvenile survival but not adult annual survival. Immigrants introduced alleles with negative additive genetic effects on local fitness, potentially reducing population mean fitness through migration load, but alleviating expression of inbreeding depression. Our results show that V for fitness can be maintained in the wild, and be broadly concordant between the sexes despite marked sex-specific V in reproductive success.

Individuals’ expected genetic contributions to future generations, reproductive value, and short-term metrics of fitness in free-living song sparrows (Melospiza melodia)

“…Yet, realized lifetime fitness, comprising the number of offspring that was actually produced, might be envisaged as a reasonable predictor of longer term genetic contribution that captures the im-plications of initial individual-level realizations of environmental and demographic stochasticity in survival and reproductive success (e.g., Saether and Engen 2015). Predictive capability will also depend partly on the additive genetic variance and heritability in LRS, which is nonzero but small in song sparrows (<0.1 measured approximately chick-to-chick, implying that ß90% of phenotypic variation represents "stochasticity"; Wolak et al 2018). Such small or moderate values may be broadly typical, although still surprisingly few rigorous estimates are available (Shaw and Shaw 2014;Hendry et al 2018).…”

“…Perhaps the closest to broad conceptual unanimity is the idea that the "fittest" entities are ultimately those that contribute most descendants to a population at some point in the future (Benton and Grant 2000;Day and Otto 2001;Brommer et al, 2002Brommer et al, , 2004Hunt et al 2004;Grafen 2006;Roff 2008;Hunt and Hodgson 2010;Graves and Weinreich 2017). Yet, such concepts can seem remote from the short-term metrics of individual fitness that empiricists working on free-living populations commonly aim to measure, which typically comprise simple functions of individuals' realized survival and/or reproductive success (Brommer et al, 2002(Brommer et al, , 2004Link et al 2002;Coulson et al 2006;Hendry et al 2018;Wolak et al 2018). Such metrics can correctly enumerate individual contributions to the next year or generation, but will not necessarily directly predict longer term genetic contributions, especially given density-, frequency-, and/or environment-dependent selection (de Jong 1994;Day and Otto 2001;Hunt et al 2004;Roff 2008;Saether and Engen 2015;Graves and Weinreich 2017).…”

“…Such multigeneration data exist for a small, largely philopatric, population of song sparrows inhabiting Mandarte island, Canada (full details in Supporting Information S1). The available data allow calculation of any desired metric of relatedness and fitness across individuals hatched since 1992, with little uncertainty or missing data with respect to the local population (Reid et al, 2014(Reid et al, , 2016Wolak et al 2018, Supporting Information S1).…”

“…On Mandarte, among-year variation in local environmental conditions and population density drives considerable amongyear variation in song sparrow reproduction and survival (Arcese et al 1992;Wilson and Arcese 2003;Tarwater and Arcese 2018), inducing substantial among-cohort variation in mean lifespan and LRS (Lebigre et al 2012;Wolak et al 2018). Total adult population size consequently varied substantially among years (arithmetic mean: 73 ± 29 SD individuals, range: 33-128, Supporting Information S1).…”

“…However, in practice, and in other contexts, fitness is commonly measured adult-to-offspring or adult-to-adult. This includes studies that aim to quantify fitness consequences of expression of adult traits (including reproductive or secondary sexual traits) and directly infer evolutionary outcomes, or to estimate N e (e.g., Wolf and Wade 2001;Kokko et al 2003;Hunt et al 2004;MacColl and Hatchwell 2004;Saether and Engen 2015;Myhre et al 2016;Wolak et al 2018). To encompass this spectrum of approaches, we extracted six lifetime fitness metrics for each focal individual.…”