The quantitative genetics of fitness in a wild seabird

Abstract

Additive genetic variance in fitness is a prerequisite for adaptive evolution, as a trait must be genetically correlated with fitness to evolve. Despite its relevance, additive genetic variance in fitness has not often been estimated in nature. Here, we investigate additive genetic variance in lifetime and annual fitness components in common terns (Sterna hirundo). Using 28 years of data comprising approximately 6000 pedigreed individuals, we find that additive genetic variances in the zero-inflated and Poisson components of lifetime fitness were effectively zero but estimated with high uncertainty. Similarly, additive genetic variances in adult annual reproductive success and survival did not differ from zero but were again associated with high uncertainty. Simulations suggested that we would be able to detect additive genetic variances as low as 0.05 for the zero-inflated component of fitness but not for the Poisson component, for which adequate statistical power would require approximately two more decades (four tern generations) of data collection. As such, our study suggests heritable variance in common tern fitness to be rather low if not zero, shows how studying the quantitative genetics of fitness in natural populations remains challenging, and highlights the importance of maintaining long-term individual-based studies of natural populations.

Opposite-sex associations are linked with annual fitness, but sociality is stable over lifetime

“…This variation in individual sociality is positively linked with fitness in some taxa (Silk 2007; Silk et al 2009) and is therefore expected to be subject to selection (Krause and Ruxton 2002). Fitness is a relative measure of an individual’s genetic contribution to the population in the next generation, and thus, can only be represented comprehensively and precisely by measures of traits spanning an organism’s lifetime (Endler 1986; Blankenhorn 2010; Reid et al 2019; Moiron, Charmantier and Bouwhuis 2022). A comprehensive definition of fitness is fundamental to understand the evolutionary pressures that shape variation in sociality.…”

“…Whereas, in birds, the subject of this study, the use of fitness correlates (eggs laid, chicks fledged, within-year survival etc.) are frequent against more precise fitness measures (Moiron, Charmantier and Bouwhuis 2022), that require intensive field work over a long period of time.…”

Opposite-sex associations are linked with annual fitness, but sociality is stable over lifetime

“…This variation in individual sociality is positively linked with fitness in some taxa ( Silk 2007 ; Silk et al 2009 ) and is therefore expected to be subject to selection ( Krause and Ruxton 2002 ). Fitness is a relative measure of an individual’s genetic contribution to the population in the next generation, and thus, can only be represented comprehensively and precisely by measures of traits spanning an organism’s lifetime ( Endler 1986 ; Blankenhorn 2010 ; Reid et al 2019 ; Moiron et al 2022 ). A comprehensive definition of fitness is fundamental to understand the evolutionary pressures that shape variation in sociality.…”

“…Whereas, in birds, the subject of this study, the use of fitness correlates (eggs laid, chicks fledged, within-year survival, etc.) are frequent over more precise fitness measures ( Moiron et al 2022 ), that require intensive field work over a long period of time.…”

Divorce is linked with extra‐pair paternity in a monogamous passerine

“…First, the heritability of male and female promiscuity is often near zero, and closely related to fitness, potentially masking any evidence of pleiotropy effect (Reid et al 2011, Reid 2015, Dobson et al 2023). And second, studies with genetic pedigrees from wild populations are scarce and have few generations, resulting in inconclusive effect sizes (Reid et al 2011, Moiron et al 2022, Dobson et al 2023), even where prevalence of extra‐pair behaviour is high. However, if pleiotropic effects are driving female extra‐pair behaviour then the expression of two linked behaviours should be empirically – if not genetically – detectable in wild systems.…”