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

Abstract

Ongoing adaptive evolution, and resulting “evolutionary rescue” of declining populations, requires additive genetic variation in fitness. Such variation can be increased by gene flow resulting from immigration, potentially facilitating evolution. But, gene flow could in fact constrain rather than facilitate local adaptive evolution if immigrants have low additive genetic values for local fitness. Local migration-selection balance and micro-evolutionary stasis could then result. However, key quantitative genetic effects of natural immigration, comprising the degrees to which gene flow increases the total local additive genetic variance yet counteracts local adaptive evolutionary change, have not been explicitly quantified in wild populations. Key implications of gene flow for population and evolutionary dynamics consequently remain unclear. Our quantitative genetic analyses of long-term data from free-living song sparrows (Melospiza melodia) show that mean breeding value for local juvenile survival to adulthood, a major component of fitness, increased across cohorts more than expected solely due to drift. Such micro-evolutionary change should be expected given nonzero additive genetic variance and consistent directional selection. However, this evolutionary increase was counteracted by negative additive genetic effects of recent immigrants, which increased total additive genetic variance but prevented a net directional evolutionary increase in total additive genetic value. These analyses imply an approximate quantitative genetic migration-selection balance in a major fitness component, and hence demonstrate a key mechanism by which substantial additive genetic variation can be maintained yet decoupled from local adaptive evolutionary change.

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

“…Phenotypic changes in migration may also arise plastically and influence subsequent genetic change (Coppack & Pulido, 2004; Pulido, 2007; Teplitsky & Millien, 2014). Quantitative genetic approaches (Kruuk, 2004; Wolak et al, 2018; Reid et al, 2021) to estimate the genetic basis of partial migration and pedigree-based comparison of individuals displaying different migratory tactics should also help elucidate the contributions of phenotypic plasticity versus micro-evolution in local adaptation to rapid environmental change.…”

Are immigrants outbred and unrelated? Testing standard assumptions in a wild metapopulation

“…This sample includes individuals that hatched on or immigrated to Mandarte during 1993-2013, alongside some surviving individuals that hatched or arrived in earlier years. Previous analyses of resulting pedigree data showed that mean f varied little across years (Reid et al, 2021), with no evidence of non-random mating with respect to…”

“…This article is protected by copyright. All rights reserved Reid et al, 2014Reid et al, , 2015Reid et al, , 2016 , and the quantitative genetic basis of life-history variation (Reid, Arcese, Sardell, & Keller, 2011;Reid & Sardell, 2012;Wolak et al, 2018), including consequences of immigration (Marr et al, 2002;Reid & Arcese, 2020;Reid et al, 2021;Wolak et al, 2018). Recent analyses utilized complete multi-year pedigree data, where genetic parentage of focal Mandarte-hatched individuals was verified with very high statistical confidence (Nietlisbach et al, 2017;Reid et al, 2011Reid et al, , 2014Reid et al, , 2021Sardell, Keller, Arcese, Bucher, & Reid, 2010) .…”

“…migration load, Bolnick & Nosil, 2007;Garant et al, 2007;Lenormand, 2002) . Understanding the diverse genetic impacts of immigration is therefore central to understanding evolutionary dynamics in metapopulation systems (Carlson, Cunningham, & Westley, 2014;Garant et al, 2007;Lenormand, 2002;Reid et al, 2021) , predicting fates of populations experiencing changing environments (Aitken & Whitlock, 2013) , conservation of small inbred populations (Frankham, 2015) , and optimal animal breeding (Fernández et al, 2012;Rudnick & Lacy, 2008) Theoretical and empirical studies in all these research areas commonly make three standard assumptions regarding genetic properties of new immigrants into any focal…”

The quantitative genetics of fitness in a wild seabird

“…For instance, the study of Wolak et al (2018) on the song sparrow population of Mandarte Island reported evidence of non-zero VA for juvenile survival. The natural history of common terns and song sparrows differ in many ways, yet one reason for this disparity could be a difference in emigration rates since the Mandarte population is isolated with very little juvenile emigration (Reid et al 2021).…”