Genetic evidence challenges the native status of a threatened freshwater fish (Carassius carassius) in England

Abstract

A fundamental consideration for the conservation of a species is the extent of its native range, that is, regions naturally colonized. However, both natural processes and human-mediated introductions can drive species distribution shifts. Ruling out the human-mediated introduction of a species into a given region is vital for its conservation, but remains a significant challenge in most cases. The crucian carp Carassius carassius (L.) is a threatened freshwater fish thought to be native to much of Europe.However, its native status in England is based only on anecdotal evidence. Here, we devise an approach that can be used to empirically test the native status of English fauna. We use this approach, along with 13 microsatellite loci, population structure analyses, and Approximate Bayesian Computation (ABC), to test hypotheses for the origins of C. carassius in England. Contrary to the current consensus, we find strong support for the human-mediated introduction of C. carassius into England during the 15th century. This result stimulates an interesting and timely debate surrounding motivations for the conservation of species. We discuss this topic, and the potential for continued conservation of C. carassius in England, despite its non-native origins. K E Y W O R D SApproximate Bayesian Computation, introduced species, land bridge, microsatellites, postglacial recolonization | INTRODUCTIONObtaining a detailed understanding of a species' native range and the distribution of its diversity within that range is fundamental for species conservation (Frankham, Briscoe, & Ballou, 2002; IUCN 2016;Reed & Frankham, 2003;Scoble & Lowe, 2010). A species is usually considered native if it has colonized an area naturally, whereas it is considered non-native in areas which have been colonized with human intervention (Copp et al., 2005;Gozlan, Britton, Cowx, & Copp, 2010).Species' ranges are not static but often change dramatically over time in response to changing environments, newly-arising dispersal corridors and human-mediated factors. During the last 2.5 MY, the ranges of European biota have been most strongly impacted by glacial cycles (Hewitt, 1999). These processes have been extensively studied, particularly in freshwater fishes, whose postglacial recolonization dynamics have been determined by the history of river drainage systems (Bănărescu, 1990(Bănărescu, , 1992Bernatchez & Wilson, 1998;Bianco, 1990;Hänfling & Brandl, 1998;Jeffries et al., 2016;Reyjol et al., 2006). For example, ephemeral rivers and periglacial lakes that result from glacial meltwater have provided opportunities for fish colonizations (Gibbard, Rose, & Bridgland, 1988) of otherwise isolated drainages (Arkhipov, Ehlers, Johnson, & Wright, 1995;Grosswald, 1980). However, the 2872 | JEEFRJES Jet al current distributions of European freshwater fishes have also been significantly impacted by human-mediated translocations, which have enabled some species to overcome natural dispersal barriers like watersheds (Copp et al., 2005;Gozlan et al., 2010). ...

At what spatial scale should risk screenings of translocated freshwater fishes be undertaken - River basin district or climo-geographic designation?

“…The species included in the list of translocated freshwater fishes encompassed: A) all native species that are known to have been introduced from their native distribution range in GB to other parts of GB where the species is not native; and B) any other native species likely to be translocated within GB. Note that in the case of crucian carp Carassius carassius, the RA area encompasses all parts of GB because a recent genetic study has demonstrated that this species was most likely introduced about the same time as common carp Cyprinus carpio, and therefore is most likely 'not native' to southeast England as was previously believed by some scientists (Jeffries et al, 2017). A similar approach, encompassing both extant and potential future species, has been used in all published applications of AS-ISK on freshwater fishes to date (i.e., Glamuzina et al, 2017;Li et al, 2017; and in most previous applications of FISK (see Copp, 2013), as this provides a means of assessing current species, which may or may not have expressed invasive patterns.…”

Development and application of environmental DNA surveillance for the threatened crucian carp (Carassius carassius)

“…Conservation organisations (e.g. English Nature, Environment Agency) later recognised the crucian carp as native and threatened (Environment Agency, ; Smith & Moss, ), but recent genetic evidence supports anthropogenic introduction of the crucian carp to the UK during the 15th century (Jeffries et al., ). Nonetheless, many introduced species in the UK are now naturalised, and several provide ecological and economical benefits (Manchester & Bullock, ).…”

Phylogeography of the highly invasive sugar beet nematode, Heterodera schachtii (Schmidt, 1871), based on microsatellites

“…Three pooled populations were considered in this step, based on the three STRUCTURE‐defined groups: NE, TU (TU_AK and TU_NI), and CORE (UK, US_CA, US_OR, AU, GE, and IR). Pooling populations with shared history is an efficient way to reduce the complexity of candidate scenarios and has been used in numerous other studies (see Pedreschi et al, ; Jeffries et al, ). Six evolutionary scenarios that considered population history events including divergence, admixture, and population size variation were evaluated.…”