The marbled crayfish as a paradigm for saltational speciation by autopolyploidy and parthenogenesis in animals.

Günter Vogt,Mark Helm,Ralf Schulz,Frank Lyko,Katharina Hanna,Katharina Schmid,Anne Schrimpf,Jörn Panteleit,Cassandra Falckenhayn

doi:10.1242/bio.014241

Abstract

ABSTRACTThe parthenogenetic all-female marbled crayfish is a novel research model and potent invader of freshwater ecosystems. It is a triploid descendant of the sexually reproducing slough crayfish, Procambarus fallax, but its taxonomic status has remained unsettled. By cross-breeding experiments and parentage analysis we show here that marbled crayfish and P. fallax are reproductively separated. Both crayfish copulate readily, suggesting that the reproductive barrier is set at the cytogenetic rather than the behavioural level. Analysis of complete mitochondrial genomes of marbled crayfish from laboratory lineages and wild populations demonstrates genetic identity and indicates a single origin. Flow cytometric comparison of DNA contents of haemocytes and analysis of nuclear microsatellite loci confirm triploidy and suggest autopolyploidisation as its cause. Global DNA methylation is significantly reduced in marbled crayfish implying the involvement of molecular epigenetic mechanisms in its origination. Morphologically, both crayfish are very similar but growth and fecundity are considerably larger in marbled crayfish, making it a different animal with superior fitness. These data and the high probability of a divergent future evolution of the marbled crayfish and P. fallax clusters suggest that marbled crayfish should be considered as an independent asexual species. Our findings also establish the P. fallax–marbled crayfish pair as a novel paradigm for rare chromosomal speciation by autopolyploidy and parthenogenesis in animals and for saltational evolution in general.

Highlights

Crossbreeding experiments and parentage analysis Crossbreeding experiments were performed to investigate whether marbled crayfish and P. fallax can interbreed and produce viable offspring
P. alleni males copulated neither with P. fallax nor with marbled crayfish females (Table 1) suggesting that they did not recognise them as sexual partners
Our results demonstrate that marbled crayfish meets all the criteria for asexual speciation, as formalised by Barraclough et al (2003) and Birky and Barraclough (2009): 1) The marbled crayfish is separated from its mother species, P. fallax, by reproductive isolation, significant genomic and epigenetic differences and superior life history traits; 2) Our data support a single origin of all marbled crayfish; 3) All populations known to date live outside the natural range of P. fallax, suggesting geographical isolation; and 4) All marbled crayfish populations are unified in one cluster by common phenotypic, genetic and epigenetic characteristics, despite their broad geographical distribution

Summary

Introduction

Marbled crayfish is the only known obligatory parthenogen among the ∼15,000 decapod crustaceans. It was discovered in 1995 in the German aquarium trade (Vogt, 2008a) and has become a popular pet in Europe and other continents since (Chucholl, 2014; Faulkes, 2015b). By comparison of morphological traits and molecular markers, Martin et al (2010) have identified the sexually reproducing slough crayfish Procambarus fallax from Florida and southern Georgia as the mother species of marbled crayfish. Several important characteristics of marbled crayfish have been described in detail, including morphology (Kawai et al, 2009), embryonic development (Seitz et al, 2005; Alwes and Scholtz, 2006), life history (Vogt et al, 2004; Seitz et al, 2005; Vogt, 2008b, 2010), parthenogenetic reproduction (Scholtz et al, 2003; Martin et al, 2007; Vogt et al, 2008) and a triploid karyotype (Martin et al, 2015)

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Discussion

Conclusion