Genomic footprints of a biological invasion: introduction from Asia and dispersal in Europe of the topmouth gudgeon (Pseudorasbora parva)

Facilitated by the intensification of global trading, the introduction and dispersal of species to areas in which they are historically non-native is nowadays common. From an evolutionary standpoint, invasions are paradoxical: not only non-native environments could be different from native ones for which introduced individuals would be ill-adapted, but also small founding population size should be associated with reduced adaptive potential. As such, biological invasions are considered valuable real-time evolutionary experiments. Here, we investigated the population structure and adaptive potential of the highly invasive topmouth gudgeon (Pseudorasbora parva) across Europe and East Asia. We RAD-sequenced 301 specimens from sixteen populations and three distinct within-catchment invaded regions as well as two locations in the native range. With 13785 single nucleotide polymorphisms, we provide conclusive evidence for a genome-wide signature of two distinct invasion events, in Slovakia and Turkey, each originating from a specific area in the native range. A third invaded area, in France, appears to be the result of dispersal within the invasive range. Few loci showed signs of selection, the vast majority of which being identified in the Slovakian region. Functional annotation suggests that faster early stage development, resistance to pollution and immunocompetence contribute to the invasion success of the local habitats. By showing that populations in the invasive range have different evolutionary histories, our study reinforces the idea that populations, rather than species, are the units to consider in invasion biology.

随着全球贸易的日益深化，物种被引入并扩散至其历史分布范围以外的区域已成为普遍现象。从进化生物学视角来看，生物入侵本身存在矛盾：一方面，非原生境与物种的原生境存在显著差异，引入的个体往往适应性不佳；另一方面，较小的奠基种群规模通常会导致群体的进化潜力降低。正因如此，生物入侵被视为极具价值的实时进化实验体系。本研究针对分布于欧洲与东亚的高入侵性物种麦穗鱼（topmouth gudgeon, Pseudorasbora parva）的种群结构与进化潜力展开探究。我们对来自16个种群、3个流域内入侵区域以及2个原生分布区域的301个样本进行了RAD-seq测序。基于13785个单核苷酸多态性（SNP）位点，我们的研究为欧洲斯洛伐克与土耳其地区的两次独立入侵事件提供了全基因组水平的确凿证据，这两次入侵的源头均来自东亚原生分布区的特定区域。而位于法国的第三个入侵区域，则似乎是入侵范围内种群扩散的结果。仅有少量基因座呈现出选择信号，其中绝大多数均在斯洛伐克种群中被检测到。功能注释分析结果表明，更快的早期发育速度、更强的抗污染能力以及更高的免疫活性，助力该物种成功入侵当地生境。本研究证实入侵区域内的不同种群拥有独特的进化历史，这进一步强化了入侵生物学领域的核心观点：在入侵生物学研究中，应当以种群而非物种作为研究单元。