Population assignment reveals low migratory connectivity in a weakly structured songbird

Abstract

Understanding migratory connectivity is essential for determining the drivers behind population dynamics and for implementing effective conservation strategies for migratory species. Genetic markers provide a means to describe migratory connectivity; however, they can be uninformative for species with weak population genetic structure, which has limited their application. Here, we demonstrated a genomic approach to describing migratory connectivity in the prothonotary warbler, Protonotaria citrea, a Neotropical songbird of conservation concern. Using 26,189 single nucleotide polymorphisms (SNPs), we revealed regional genetic structure between the Mississippi River Valley and the Atlantic Seaboard with overall weak genetic differentiation among populations (F ST = 0.0055; 95% CI: 0.0051-0.0059). Genetic variation had a stronger association with geographic rather than environmental factors, with each explaining 14.5% and 8.2% of genetic variation, respectively. By varying the numbers of genomic markers used in population assignment models with individuals of known provenance, we identified a maximum assignment accuracy (89.7% to site, 94.3% to region) using a subset of 600 highly differentiated SNPs. We then assigned samples from nonbreeding sites to breeding region and found low migratory connectivity. Our results highlight the importance of filtering markers for informative loci in models of population assignment. Quantifying migratory connectivity for weakly structured species will be useful for expanding studies to a wider range of migratory species across taxonomic groups and may contribute to a deeper understanding of the evolution of migratory strategies. K E Y W O R D S ddRADseq, migratory connectivity, population assignment, population genetics, Protonotaria citrea, redundancy analysis 1 | INTRODUC TI ON Migratory species are declining in abundance globally and represent a unique challenge for conservation planning (Robinson et al., 2009; Runge, Martin, Possingham, Willis, & Fuller, 2014). Understanding the spatial connections of populations throughout the full annual cycle is critical for understanding the ecology and evolutionary biology of migratory species and informing effective management decisions aimed at reversing declines (Faaborg et al.,

Using multiple natural tags provides evidence for extensive larval dispersal across space and through time in summer flounder

“…Genetically diverged candidate loci contain higher information content, allowing greater assignment accuracy than would be possible using an equal or greater number of neutral loci. For example, Freamo et al (2011) achieved 85% assignment accuracy when using 14 candidate outlier loci compared to 75% assignment accuracy when using 67 neutral loci in salmon, and studies in other systems have achieved equal success using many more markers (Benestan et al, 2015; DeSaix et al, 2019; Rannala & Mountain, 1997). The 10 candidate outlier loci available for summer flounder were differentiated across geography, but only weakly so, which resulted in low power to assign individuals to populations of origin.…”

“…Low genetic differentiation at neutral markers has limited efficacy for population assignment because of ongoing gene flow. However, candidate outlier loci, or gene‐associated markers, that arise due to divergent environmental selection are promising for population assignment because of their elevated differentiation compared to neutral markers (Benestan et al, 2015; DeSaix et al, 2019; Freamo et al, 2011; Nielsen et al, 2009, 2012). Genetically diverged candidate loci contain higher information content, allowing greater assignment accuracy than would be possible using an equal or greater number of neutral loci.…”

Bergmann's rule is followed at multiple stages of postembryonic development in a long‐distance migratory songbird

“…As body size is strongly related to important traits such as thermoregulatory (especially at such early post‐embryonic stages) and migratory ability, it would seem likely that there is at least some genetic basis for these patterns. However, a recent study of the population genomics of prothonotary warblers found little latitudinal population structure (but greater longitudinal variation, possibly related to geographic isolation between migratory pathways; DeSaix et al., 2019). This genomic work, however, was not designed to detect genetic differences related to body mass variation.…”

“…Prothonotary warblers have an incubation period of 11–14 days, fledging occurs 9–11 days following hatching (Petit, 1999), and they can produce up to three broods in a season. Recent studies of geographic variation in the species (on the breeding grounds) have identified weak longitudinal genetic population structure (DeSaix et al., 2019) and variation in color and sexual signaling (Slevin, Bulluck, Matthews, & Boves, 2019). During the non‐breeding season, the bulk of the global population appears to winter in a relatively small area in Colombia and Panama (Reese et al., 2019; Tonra et al., 2019).…”

“…We modeled each developmental stage (egg, early nestling, late nestling, and adults) independently and qualitatively compared patterns across stages. First, we used body mass (or egg dimensions; length and width) as a continuous dependent variable, and treated latitude and longitude (to account for potential geographical differences as described by Slevin et al., 2018 and DeSaix et al., 2019), year, age (nestlings: days since hatching, adults: SY or ASY), and ambient temperature as independent fixed effects, and sampling time, date, and nest ID (to account for multiple eggs/nestlings in the same clutch or brood) as random effects (included in all models). For adult birds, we also included sex as a categorical fixed effect.…”