Whole‐genome sequencing reveals small genomic regions of introgression in an introduced crater lake population of threespine stickleback

Abstract

Invasive species pose a major threat to biological diversity. Although introduced populations often experience population bottlenecks, some invasive species are thought to be originated from hybridization between multiple populations or species, which can contribute to the maintenance of high genetic diversity. Recent advances in genome sequencing enable us to trace the evolutionary history of invasive species even at whole‐genome level and may help to identify the history of past hybridization that may be overlooked by traditional marker‐based analysis. Here, we conducted whole‐genome sequencing of eight threespine stickleback (Gasterosteus aculeatus) individuals, four from a recently introduced crater lake population and four of the putative source population. We found that both populations have several small genomic regions with high genetic diversity, which resulted from introgression from a closely related species (Gasterosteus nipponicus). The sizes of the regions were too small to be detected with traditional marker‐based analysis or even some reduced‐representation sequencing methods. Further amplicon sequencing revealed linkage disequilibrium around an introgression site, which suggests the possibility of selective sweep at the introgression site. Thus, interspecies introgression might predate introduction and increase genetic variation in the source population. Whole‐genome sequencing of even a small number of individuals can therefore provide higher resolution inference of history of introduced populations.

Multiple waves of freshwater colonization of the three-spined stickleback in the Japanese Archipelago

“…For example, non-native populations from FW Kobe [K] and FW Komono [J] were derived from either Aizu or FW Nasu [u] populations. Although non-native populations can provide opportunities to study the process of adaptation to novel habitats on a contemporary timescale [27,28], their spread may lead to hybridization with, or extinction, of native populations [24]. Native freshwater populations are invaluable genetic resources to study the genetic basis of adaptive phenotypic diversi cation generated during the last 200,000 years in the Japanese Archipelago.…”

“…For G. aculeatus collected from Akkeshi [d], G. nipponicus from the population Akkeshi [Q], and Gasterosteus wheatlandi, we used the sequences determined [65]. Sequence data of G. aculeatus from Aisaka [B] and Lake Towada [D] were derived from a previous study [28]. For G. aculeatus from northern Europe, the sequences of two randomly selected samples from the marine population reported previously [66], and those of one or two randomly selected samples from each freshwater population reported previously [67] were obtained.…”

“…These freshwater populations are not genetically differentiated from marine G. aculeatus at allozyme or microsatellite loci [25,26]. Several humanintroduced populations also offer opportunities to investigate the genetic basis of rapid adaptation [27,28]. Freshwater populations with such a diverse array of colonization ages provide opportunities to investigate how freshwater adaptation progresses over time.…”

“…G. aculeatus has higher copy numbers of the metabolic gene Fads2 and can survive better on freshwater-derived diets than G. nipponicus [18]. Because there is past and ongoing hybridization between these two species [28,[32][33][34], it is important to determine the extent of introgression of freshwater-adaptive alleles between these two species to understand the genetic factors constraining the freshwater colonization of G. nipponicus.…”

Chromosome-level genome construction of a Japanese stickleback species using ultra-dense linkage analysis using single-cell sequencing of sperms

“…In this study, single-cell whole genome amplification is performed on sperms of Gasterosteus nipp onicus using 10x single-cell genome (CNV) sequencing libraries. The genome size of Gasterosteus nipponicus is 465 Mb, which is relatively small among vertebrates and has been the focus of attention in the study of freshwater penetration of fishes (Ishikawa et al, 2019;Yoshida et al, 2016) and is a closely related species of the extensively studied three-spined stickleback (Gasterosteus aculeatus) (Jones e t al., 2012; Kingsley and Peichel, 2006).…”