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Potential Impact of Genome Exclusion by Alien Species in the Hybridogenetic Water Frogs (Pelophylax Esculentus Complex)

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Potential Impact of Genome Exclusion by Alien Species in the Hybridogenetic Water Frogs (Pelophylax Esculentus Complex) See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/227011487 Potential impact of genome exclusion by alien species in the hybridogenetic water frogs (Pelophylax esculentus complex) Article in Biological Invasions · January 2009 DOI: 10.1007/s10530-009-9427-2 CITATIONS READS 49 599 2 authors, including: Robert Jooris Research Institute for Nature and Forest 28 PUBLICATIONS 161 CITATIONS SEE PROFILE Some of the authors of this publication are also working on these related projects: Analysis of scutellation in populations of Cerastes vipera (Linnaeus, 1758): Scale characters co-vary with environmental temperature View project INVEXO View project All content following this page was uploaded by Robert Jooris on 25 April 2016. The user has requested enhancement of the downloaded file. Biol Invasions (2010) 12:1–13 DOI 10.1007/s10530-009-9427-2 PERSPECTIVES AND PARADIGMS Potential impact of genome exclusion by alien species in the hybridogenetic water frogs (Pelophylax esculentus complex) G. Holsbeek Æ R. Jooris Received: 23 January 2008 / Accepted: 12 January 2009 / Published online: 30 January 2009 Ó Springer Science+Business Media B.V. 2009 Abstract Globalization and increasing human water frogs in Western Europe have become frequent impact on natural aquatic systems have facilitated the last decade leading to rapid expansion of the the movement of species and the establishment of range of the marsh frog P. ridibundus. Subsequent nonindigenous species enhancing hybridisation hybridisation of the exotic P. ridibundus may opportunities between naturally allopatric species. dramatically affect the viability and maintenance of In this review, we focus on a special case of natural hybrid water frog populations throughout Europe. hybrid speciation and the consequences of recent Interestingly, the impact of this introduced species anthropogenic hybridisation in the water frog com- may differ depending on their geographic origin, plex (Pelophylax esculentus complex), which consists which defines the ability to induce genome elimina- of two parental species, Pelophylax lessonae and tion. This may result in fertile or sterile hybrids, Pelophylax ridibundus and a hybrid taxon. The making global conservation guidelines challenging. hybrid water frogs reproduce hybridogenetically and We predict a severe genetic and ecological impact of eliminate the genome of the syntopic water frog nonindigenous P. ridibundus prompting for strict species. Although the actual cause triggering chro- conservation measures to reduce species transloca- mosome exclusion remains elusive, it has been tions and for studies on the geographic origin of proposed that chromosome elimination takes place exotic frog species. prior to meiosis and may involve enzymatic degra- dation of the discarded genome. Translocations of Keywords European water frogs Á Hybrid complex Á Hybridisation Á Pelophylax ridibundus Á Translocations G. Holsbeek (&) Laboratory of Aquatic Ecology and Evolutionary Biology, Katholieke Universiteit Leuven, Ch. Deberiotstraat, 32, 3000 Louvain, Belgium Introduction e-mail: [email protected] Translocations of alien species, habitat modifications G. Holsbeek Laboratory of Animal Diversity and Systematics, and fragmentation are the primary factors that are Katholieke Universiteit Leuven, Ch. Deberiotstraat, believed to contribute to the current increase of 32, 3000 Louvain, Belgium hybridisation rates between naturally allopatric spe- cies (Allendorf et al. 2001; Frankham et al. 2002; R. Jooris Natuurpunt, Michiel Coxiestraat 11, Rhymer and Simberloff 1996). Global trade has 2800 Mechlin, Belgium facilitated the movement of species outside their 123 2 G. Holsbeek, R. Jooris natural environment and enhanced the establishment frog species (Arano et al. 1995; Grossenbacher 1988; of nonindigenous species in new habitats (Mooney Holsbeek et al. 2008; Pagano et al. 2001a, 2003; and Cleland 2001), increasingly putting pressure on Vorburger and Reyer 2003). The water frog complex indigenous species already suffering from human- forms a suitable model system to investigate the induced habitat loss and fragmentation (Fahrig 2003; population genetics of alien species and translocation Forester and Machlist 1996; Pimm and Raven 2000). effects in a hybrid complex, because the unique way The establishment of invading species in new habitats of hybridogenetic reproduction allows for very rapid may result in maladaptive hybridisation with autoch- introgression between native and exotic species thonous species and genetic pollution, ultimately (Holsbeek et al. 2008; Pagano et al. 2003). Studies leading to the extinction of native species (Rhymer on hybridisation events through translocation in and Simberloff 1996). Translocation of nonindige- hybridogenetic species are necessary to design more nous species may cause outbreeding depression in suitable conservation policies for these species. In native populations, because reproductive efforts are order to identify and interpret the possible ecological wasted on producing hybrids with reduced fitness or and/or genetic consequences of introductions in the even sterile offspring (Levin et al. 1996; Rhymer and native water frog species, it is crucial to fully Simberloff 1996). Alternatively, hybridisation may understand the hybridogenetic reproduction of the positively influence species diversification in animals water frog complex and the genetic mechanism (Dowling and Secor 1997; Grant and Grant 1992; underlying hybridogenesis. We provide an overview Mooney and Cleland 2001; Seehausen 2004). Inter- of the hybridogenetic reproduction of the water frog specific hybridisation may increase genetic diversity complex. We then discuss the potential impact of more rapidly than through mutations, and populations translocated populations of members of this hybrid with high genetic diversity are expected to be on complex on the native species. average better equipped to cope with and adapt to environmental changes and diseases than populations with lower genetic diversity (Dowling and Secor The water frog complex 1997; Ellstrand and Schierenbeck 2006; Frankham et al. 2002; Seehausen 2004; Tsutsui et al. 2000). The Pelophylax esculentus complex, formerly known Since natural hybridisation is an evolutionary as Rana esculenta complex (Dubois 1992; Frost et al. process, natural hybrids are believed to be eligible 2006), consists of two parental species, Pelophylax for protection, while hybrids resulting from human ridibundus Pallas 1771 (genotype RR) and Pelophy- actions are not (Allendorf et al. 2001). It is therefore lax lessonae Camerano 1882 (genotype LL), and the of primary importance to distinguish between natural hybrid species P. kl. esculentus Linnaeus 1758 and anthropogenic hybridisation. The consequences (genotype RL, Berger 1988; Graf and Polls Pelaz of natural and anthropogenic hybridisation on native 1989). Whereas other hybridogenetic species are species have been extensively investigated (e.g. characterized by all-female and diploid hybrid pop- Arnold 2004; Grant and Grant 2002; Huxel 1999; ulations, the hybridogenetic water frog complex is Lamont et al. 2003; Mallet 2005; Rieseberg 1997). In unique due to the presence of female as well as male the present review, we focus on a special case, being hybrids (Dubois and Gu¨nther 1982; Graf and Polls anthropogenic hybridisation taking place in a hybrid Pelaz 1989). Multiple fertilisation experiments per- complex that originated from a hybridisation event in formed by Berger (1967) revealed the extraordinary the past. We discuss the water frog complex and reproductive strategy in P. kl. esculentus. The enquire to what extent hybridisation through translo- hybridogenetic nature of reproduction in the hybrid cation may have an effect in hybrid populations frogs of this complex (Berger 1973) was recognized a where natural hybridisation has occurred or is still few years later after the definition of the term occurring. Are hybrid species at risk as a result of ‘hybridogenesis’ by Schultz (1969). anthropogenic hybridisation? Natural interspecific hybrid lineages that persist The native water frog populations of Western and through hybridogenetic reproduction are widespread Central Europe have recently been subjected to among the European water frogs (Berger 1988; Graf multiple and recurrent introductions of other water and Polls Pelaz 1989). Hybrid gametogenesis in the 123 Hybridisation in a hybrid complex 3 P. esculentus complex shows peculiar geographical offspring of P. kl. esculentus inter se matings and variation. The hybridogenetic system can be catego- the operation of the ratchet (Berger 1967; Binkert rized into three major breeding strategies (Fig. 1): et al. 1982; Ogielska 1994b; Uzzell et al. 1980; the P. lessonae—P. kl. esculentus (L–E) system, the Vorburger 2001c). Vorburger (2001a, b) and Geux P. ridibundus—P. kl. esculentus (R–E) system, and et al. (2002) also revealed that P. ridibundus tadpoles all-hybrid (E) populations (Graf and Polls Pelaz from matings between P. kl. esculentus individuals 1989). The L–E system (P. lessonae—P. kl. escu- with two different ridibundus genomes survived. lentus; Fig. 1), which inhabits Western Europe, is the Even though most offspring of matings between two most widespread hybridogenetic system, and its P. kl. esculentus with the same ridibundus genomes breeding strategy has been studied to the greatest are nonviable, a low percentage (3%) of viable detail. In this
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