Recent immigrants alter the quantitative genetic architecture of paternity in song sparrows

Abstract

Quantifying additive genetic variances and cross-sex covariances in reproductive traits, and identifying processes that shape and maintain such (co)variances, is central to understanding the evolutionary dynamics of reproductive systems. Gene flow resulting from among-population dispersal could substantially alter additive genetic variances and covariances in key traits in recipient populations, thereby altering forms of sexual conflict, indirect selection, and evolutionary responses. However, the degree to which genes imported by immigrants do in fact affect quantitative genetic architectures of key reproductive traits and outcomes is rarely explicitly quantified. We applied structured quantitative genetic analyses to multiyear pedigree, pairing, and paternity data from free-living song sparrows (Melospiza melodia) to quantify the differences in mean breeding values for major sexspecific reproductive traits, specifically female extra-pair reproduction and male paternity loss, between recent immigrants and the previously existing population. We thereby quantify effects of natural immigration on the means, variances, and cross-sex covariance in total additive genetic values for extra-pair paternity arising within the complex socially monogamous but genetically polygynandrous reproductive system. Recent immigrants had lower mean breeding values for male paternity loss, and somewhatlower values for female extra-pair reproduction, than the local recipient population, and would therefore increase the emerging degree of reproductive fidelity of social pairings. Furthermore, immigration increased the variances in total additive genetic values for these traits, but decreased the magnitudes of the negative cross-sex genetic covariation and correlation below those evident in the existing population. Immigration thereby increased the total additive genetic variance but could decrease the magnitude of indirect selection acting on sex-specific contributions to paternity outcomes. These results demonstrate that dispersal and resulting immigration and gene flow can substantially affect quantitative genetic architectures of complex local reproductive systems, implying that comprehensive theoretical and empirical efforts to understand mating system dynamics will need to incorporate spatial population processes.

Immigration counter-acts local micro-evolution of a major fitness component: Migration-selection balance in free-living song sparrows

“…2016; Wolak et al. 2018; Reid and Arcese 2020). Briefly, song sparrows are primarily socially monogamous open‐nesting passerines.…”

“…2018; Muff et al. 2019; Reid and Arcese 2020). Such models can extend standard pedigree‐based quantitative genetic analyses by defining distinct groups of recent immigrants and native founders, and thereby explicitly estimate the additive genetic effects of immigrants.…”

“…Equation implies that immigration will increase the variance in total additive genetic value (V U , i.e., the population variance in u i ) above V A (i.e., the population variance in a i ) as long as g≠0 and there is some among‐individual variance in q i (Reid and Arcese 2020; Supporting Information S1). While breeding values a i are typically assumed to be normally distributed, Equation also implies that the distribution of total additive genetic values u i could be skewed, to a degree that also depends on g and the variance and skew of q i (Supporting Information S1).…”

Seasonal migration as a life history trait facilitating adaptation to climate change

“…Nestlings were uniquely color-banded after hatching, observed to independence from parental care (∼24-32 days of age), and recorded as having recruited to or disappeared from the population in late April the following year. High annual re-sighting probabilities (> 99%; Wilson et al, 2007), the enumeration of immigrants by color-banding (< 0.5 female/yr on average; Reid & Arcese 2020), continuous monitoring of breeding activity, and genetic confirmation of a 50:50 sex ratio at hatching (Postma et al, 2011) facilitated high precision in our estimates of survival, reproduction, and population growth. For simplicity, we only considered females when estimating demographic rates and population growth here (Arcese et al, 1992; Arcese & Marr, 2006).…”

“…Song sparrows are among the most polytypic vertebrates known (Aldrich, 1984;Arcese et al, 2002;Patten & Pruett, 2009) and vary markedly in migration behavior and correlated behavioral, morphological and physiological traits including body dimensions (Pruett & Winker, 2010), clutch size (Johnston, 1954), and osmoregulatory capacity (Mikles et al, 2020). Song sparrows also vary predictably in traits widely recognized as adaptations to climatic variation in seasonality and primary production (Saether et al, 2016) including migratory, territorial, dispersal, and breeding behaviors, and demographic traits linked to fecundity, parental effort, and longevity (Arcese, 1989;Arcese et al, 2002;Germain & Arcese, 2014;Tarwater & Arcese, 2017;Reid & Arcese, 2020). Because many such traits have an additive genetic basis (e.g., Schluter & Smith, 1986;Wolak & Reid, 2016;Reid & Arcese, 2020), it is plausible that spatial variation in natural selection has contributed to heritable variation in migratory phenotype, as extensively described in European blackcaps (Sylvia atricapilla; e.g., Berthold, 1991;Berthold & Pulido, 1994;Delmore et al, 2020).…”