The genetic basis of dispersal in a vertebrate metapopulation

Abstract

Dispersal affects evolutionary processes by changing population size and genetic composition, influencing the viability and persistence of populations. Investigating which mechanisms underlie variation in dispersal phenotypes and whether populations harbour adaptive potential for dispersal is crucial to understanding the eco‐evolutionary dynamics of this important trait. Here, we investigate the genetic architecture of dispersal among successfully recruited individuals in an insular metapopulation of house sparrows. We use an extensive long‐term individual‐based ecological data set and high‐density single‐nucleotide polymorphism (SNP) genotypes for over 2500 individuals. We conducted a genome‐wide association study (GWAS), and found a relationship between dispersal probability and a SNP located near genes known to regulate circadian rhythm, glycogenesis and exercise performance, among other functions. However, this SNP only explained 3.8% of variance, suggesting that dispersal is a polygenic trait. We then used an animal model to estimate heritable genetic variation (σA2), which composes 10% of the total variation in dispersal probability. Finally, we investigated differences in σA2 across populations occupying ecologically relevant habitat types (farm vs. non‐farm) using a genetic groups animal model. We found different adaptive potentials across habitats, with higher mean breeding value, σA2, and heritability for the habitat presenting lower dispersal rates, suggesting also different roles of environmental variation. Our results suggest a complex genetic architecture of dispersal and demonstrate that adaptive potential may be environment dependent in key eco‐evolutionary traits. The eco‐evolutionary implications of such environment dependence and consequent spatial variation are likely to become ever more important with the increased fragmentation and loss of suitable habitats for many natural populations.

Long‐distance dispersal in the short‐distance dispersing house sparrow (Passer domesticus)

“…These types of long‐distance dispersal events highlight the potential for colonization of new habitats by house sparrows, which may be an important and hitherto overlooked part of this species success as a global colonizer and invasive species (Anderson, 2006 ; Hanson et al., 2020 ). Future studies may utilize these observations to investigate if individual phenotypic differences in, for example, morphology (Skjelseth et al., 2007 ), physiology (Nafstad et al., 2023 ; Pepke et al., 2022 ), or life‐history characteristics (Pärn et al., 2009 ; Saatoglu et al., 2024 ) underlie longer‐than‐expected dispersal distances (Tufto et al., 2005 ) in a species with very low flight efficiency (Claramunt, 2021 ). If dispersing individuals can successfully recruit into a breeding population, then they can offer a valuable genetic contribution to small, isolated, and often inbred populations (Dickel et al., 2021 ), such as these house sparrow populations habituating to island life on the northern Norwegian coast (Niskanen et al., 2020 ; Ranke et al., 2020 ).…”

“…Thus, although long‐distance dispersal happens infrequently in house sparrows, long‐distance dispersal can have major implications for gene flow across large geographic areas (Garant et al., 2007 ), which in turn may influence the rate of inbreeding (Keller et al., 2001 ), population (re)colonization and spatio‐temporal population dynamics (Baalsrud et al., 2014 ; Billing et al., 2012 ; Ranke et al., 2021 ) and adaptive and non‐adaptive population differentiation (Aase et al., 2022 ; Araya‐Ajoy et al., 2019 ; Holand et al., 2011 ; Jensen et al., 2013 ). Furthermore, long‐distance dispersal can affect estimates of fitness of dispersers compared to non‐dispersers, because of the bias in the number of recorded offspring, especially if dispersal behavior has a heritable component (Doligez & Pärt, 2008 ; Saatoglu et al., 2024 ). This study therefore reveals the biological and methodological implications of a long tail of upper values in the distribution of dispersal distances, even in an otherwise sedentary species, and therefore the need for large‐scale longitudinal field studies quantifying these rare but important dispersal events.…”