Introgressive replacement of natives by invading Arion pest slugs

Abstract

Hybridization with invasive species is one of the major threats to the phenotypic and genetic persistence of native organisms worldwide. Arion vulgaris (syn. lusitanicus) is a major agricultural pest slug that successfully invaded many European countries in recent decades, but its impact on closely related native species remains unclear. Here, we hypothesized that the regional decline of native A. rufus is connected with the spread of invasive A. vulgaris, and tested whether this can be linked to hybridization between the two species by analyzing 625 Arion sp. along altitudinal transects in three regions in Switzerland. In each region, we observed clear evidence of different degrees of genetic admixture, suggesting recurrent hybridization beyond the first generation. We found spatial differences in admixture patterns that might reflect distinct invasion histories among the regions. Our analyses provide a landscape level perspective for the genetic interactions between invasive and native animals during the invasion. We predict that without specific management action, A. vulgaris will further expand its range, which might lead to local extinction of A. rufus and other native slugs in the near future. Similar processes are likely occurring in other regions currently invaded by A. vulgaris.

Molecular and ecological signatures of an expanding hybrid zone

“…Since then, some empirical studies have emerged in support of this view, and these indicate that hybridization provides an important source of genetic variation on which selection can act and that its adaptive role is even more widespread, among both plants and animals, than previously believed (Dowling & Secor, ; Hedrick, ; Rieseberg & Wendel, ; Rius & Darling, ). Awareness is also increasing that this mixing of gene pools can in some cases lead to the potential loss or displacement of genotypically distinct species, something which can be especially problematic for rare organisms coming into contact with more abundant ones (Zemanova et al., ). Our study adds a new empirical example from a nonmodel animal species to this idea and shows that genetic introgression may be facilitating the range expansion of some hybridizing species via niche expansion.…”

Genital morphology differentiates three subspecies of the terrestrial slug Arion ater (Linnæus, 1758) s.l. and reveals a continuum of intermediates with the invasive A. vulgaris Moquin-Tandon, 1855

“…Morphological intermediates between A. vulgaris and A. ater s.l. have been reported before (FAlkneR 1981, engelke et al 2011, HAttelAnd et al 2015, zeMAnovA et al 2017, but our study provides the first thorough description of their diversity, placing them along a continuum between the parental species. One use of our enriched character set is to recognise potential hybrids that would previously have passed as one of the parental species.…”

“…and A. vulgaris try to mate with each other and sometimes transfer spermatophores reciprocally, both in the laboratory (RotH et al 2012, dReiJeRs et al 2013 and in the field (AllgAieR 2014, Reise & dReiJeRs unpublished observations). Genetic analyses of three Swiss populations also proved that hybridisation occurs frequently (zeMAnovA et al 2017). Morphological intermediates between A. vulgaris and A. ater s.l.…”

“…Woodland populations in western Germany seem often to be orange or reddish-brown (scHMid 1997, AllgAieR 2014), whereas around Görlitz the woodland populations are usually black, the typical colour of A. ater s.s. The fr haplogroup of A. rufus is the native form in the Swiss Alps but is being displaced by A. vulgaris at lower altitudes (zeMAnovA et al 2017).…”

“…A number of studies have examined its spread northwards and eastwards across Europe, its biology, its effect on the native flora and fauna, and the reasons for its success (e.g. von PRoscHwitz 1996, 1997, gRiMM 2001, AguiAR & wink 2005, KozłowsKi 2007, knoP & ReusseR 2012, slotsBo et al 2011a, b, 2012, kAPPes et al 2012, Jensen et al 2013, zeMAnovA et al 2017. Considered as one of the 100 worst invasive pest species (RABitscH 2006), it continues to spread, currently expanding its range northwards in Scandinavia and eastwards in Eastern Europe (HAttelAnd et al 2013, PăPureanu et al 2014, and references therein).…”