Anthropogenic hybridization at sea: three evolutionary questions relevant to invasive species management

Abstract

Species introductions promote secondary contacts between taxa with long histories of allopatric divergence. Anthropogenic contact zones thus offer valuable contrasts to speciation studies in natural systems where past spatial isolations may have been brief or intermittent. Investigations of anthropogenic hybridization are rare for marine animals, which have high fecundity and high dispersal ability, characteristics that contrast to most terrestrial animals. Genomic studies indicate that gene flow can still occur after millions of years of divergence, as illustrated by invasive mussels and tunicates. In this context, we highlight three issues: (i) the effects of high propagule pressure and demographic asymmetries on introgression directionality, (ii) the role of hybridization in preventing introduced species spread, and (iii) the importance of postzygotic barriers in maintaining reproductive isolation. Anthropogenic contact zones offer evolutionary biologists unprecedented large scale hybridization experiments. In addition to breaking the highly effective reproductive isolating barrier of spatial segregation, they allow researchers to explore unusual demographic contexts with strong asymmetries. The outcomes are diverse, from introgression swamping to strong barriers to gene flow, and lead to local containment or widespread invasion. These outcomes should not be neglected in management policies of marine invasive species. This article is part of the theme issue ‘Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers’.

Pre‐introduction introgression contributes to parallel differentiation and contrasting hybridization outcomes between invasive and native marine mussels

“…We observed stronger introgression asymmetries in contigs distinguishing Mediterranean and Atlantic M. galloprovincialis lineages compared to genome-wide trends in Batemans Bay, an observation consistent with M. edulis alleles influencing introgression barriers between introduced lineages (South Africa) and in secondary contact with native congeners (Batemans Bay). Genomic studies of marine invasive species and especially anthropogenic hybrid zones are still rare (Viard et al, 2016;Viard et al, 2020). The lack of strong reproductive isolation among M. galloprovincialis and M. planulatus provides a contrast to secondary contact in Ciona tunicates (Bouchemousse, Liautard-Haag, Bierne, & Viard, 2016;Viard et al, 2020) and oysters (Gagnaire et al, 2018) where reproductive isolation is strong.…”

“…Genomic studies of marine invasive species and especially anthropogenic hybrid zones are still rare (Viard et al, 2016;Viard et al, 2020). The lack of strong reproductive isolation among M. galloprovincialis and M. planulatus provides a contrast to secondary contact in Ciona tunicates (Bouchemousse, Liautard-Haag, Bierne, & Viard, 2016;Viard et al, 2020) and oysters (Gagnaire et al, 2018) where reproductive isolation is strong. Thus, in introduced-native Mytilus hybrid zones there is the opportunity to observe the earliest stages of extensive admixture that may lead to consolidation into islands of divergence or to complete genomic swamping.…”

“…Invasive species are likely to experience a variety of new ecological conditions under which they did not evolve (Colautti & Lau, 2015) and may occupy vastly diverse abiotic conditions and habitats in their introduced ranges (Guzinski, Ballenghien, Daguin-Thiébaut, Lévêque, & Viard, 2018;Tepolt, 2015). Invasive species are also likely to encounter congeneric species and gene flow may ensue if isolating barriers to reproduction are semi-permeable (Viard, David, & Darling, 2016;Viard, Riginos, & Bierne, 2020).…”

Phylogeography and the Description of Geographic Patterns in Invasion Genomics

“…These inferences need to be carefully interpreted, as some studies have suggested that artificial transport blurs the DNA signatures that are used to study biological invasions (Rius et al, 2012;David, 2018). In addition, studies of genomics patterns of biological invasions increasingly report hybridization between previously isolated genotypes due to human activities (Chunco, 2014;Viard et al, 2020). Although the recent mixing of divergent genotypes may help non-indigenous species cope better with or adapt to novel conditions found in the introduced range (Bourne et al, 2018;Blakeslee et al, 2020), it considerably obscures the interpretation of phylogeographic results.…”

Niche shifts lead to hybridization between twoAmazonaparrot sister-species introduced to Southern California

“…While most studies of anthropogenic hybridization have focused on its consequences for native species (Allendorf et al, 2004; Beninde et al, 2018; McFarlane and Pemberton, 2019; Viard et al, 2020), an equally interesting situation arises when two introduced species find themselves in a novel geographic region. This scenario—rare now, but certainly becoming more common—provides an opportunity to study how isolating factors that are extrinsic (e.g.…”