Signatures of selection in a recent invasion reveals adaptive divergence in a highly vagile invasive species

Abstract

A detailed understanding of population genetics in non-native populations helps us to identify drivers of successful introductions. However, separating adaptive change from local signatures of founding populations represents a conceptual and technical difficulty when dealing with invasive populations. The history of introductions, as well as the process of range expansion, can confound interpretation of putative adaption in response to a novel environment. Here, we investigate putative signals of selection in Australian populations of introduced common starlings, Sturnus vulgaris, by examining population wide Single Nucleotide Polymorphisms (SNPs) and identifying SNP outliers associated with environmental variables. We determine that geographic distance plays a strong role in the genetic structure of populations, and that this is most likely strongly influenced by genetic differences in the founding populations, as well as modern day population connectivity.Examining candidate SNPs under putative selection indicated that local adaption has likely occurred, however, strong patterns in genetic variation, likely from founding populations, were visible in SNPs that were strongly associated with environmental variables. When examining putative adaption in invasive populations, we encourage critical interpretation of signatures of selection. Even strongly associated loci and environmental variables, when examined closely, may contain distinct footprints of invasion history or invasion expansion gradients, confounding analysis of the history of selection in these populations.

Contrasting mitochondrial diversity of European starlings (Sturnus vulgaris) across three invasive continental distributions

“…First, previous studies of starlings in Australia, South Africa, and the UK used mitochondrial control region sequence data, so the comparative strength of our study is predicated on using the same marker. Second, Australian studies that have compared population structure using mitochondrial sequence data to that of microsatellite (Rollins et al., 2011) and single nucleotide polymorphism data (Cardilini et al, 2020) found similar patterns, supporting the validity of our approach. Third, mitochondrial DNA is still one of the most reliable sources of DNA that can be extracted from historical museum specimens (Guschanski et al., 2013; Mason, Li, Helgen, & Murphy, 2011; Ramakrishnan & Hadly, 2009), and population analyses using historical specimens rely on comparable datasets from modern birds, such as this.…”

“…The haplotype network including all populations (Figure 2 (Rollins et al, 2009(Rollins et al, , 2011 and evidence of local adaptation to the Australian environment has been described (Cardilini, Buchanan, Sherman, Cassey, & Symonds, 2016;Cardilini et al, 2020). However, in South Africa, no evidence of population structure was found (Berthouly-Salazar et al, 2013).…”

“…In Australia, up to sixteen different introduction attempts have been made with birds originating from the United Kingdom, from 1856 to 1881, with only two resulting in recorded established populations from ~165 original birds (Higgins et al, 2006; Long, 1981). Nuclear and mitochondrial markers identified concurrent population structure across the Australian range, and nuclear polymorphisms were associated with environmental variables in that population (e.g., aridity; Cardilini et al, 2020; Rollins et al., 2009, 2011). In contrast to the high levels of propagule pressure in Australia, only one introduction to South Africa of ~18 birds originating from Britain in or around 1897 has been recorded (Winterbottom & Liversidge, 1954).…”

Environmental correlates of genetic variation in the invasive and largely panmictic European starling in North America

“…In fact, starlings at the expansion front may have rapidly adapted during the Australian invasion (Rollins et al, 2016): the proportion of adult starlings in Western Australia carrying a novel mitochondrial haplotype has increased rapidly only at this range edge. A genotyping-by-sequencing survey employing a much greater number of SNP markers indicates three population subdivisions in Australia, where geographic distance explains genetic differentiation in starlings better than does environmental variation (Cardilini et al , 2020). Global F ST across all Australian populations is an order of magnitude higher than the equivalent F ST index across North America, despite similar areas sampled.…”

“…A similar project on starlings in the Australian invasion-which colonized that continent nearly concurrently with the North American invasion-found that geographic but not environmental distance explains genetic patterns there (Cardilini et al, 2020). Starlings in the Australian range show substantial population structuring and significant patterns of isolation-by-distance.…”