In-depth investigation of the species problem and taxonomic status of marbled crayfish, the first asexual decapod crustacean

Abstract

The marbled crayfish is the only obligately parthenogenetic decapod crustacean and a novel research model and invasive animal on three continents. It is regarded either as a parthenogenetic form of slough crayfish Procambarus fallax or as a separate species named Procambarus virginalis. In order to investigate the species question of this unusual crayfish in detail we have identified the similarities and differences in morphology, life history, genetics, behaviour, ecology and biogeography between marbled crayfish and P. fallax. We have investigated specimens from natural habitats, laboratory colonies and museum collections and performed a meta-analysis of our data and published data. Our COI based molecular tree with 27 Cambaridae confirms closest relationship of marbled crayfish with P. fallax. Marbled crayfish and P. fallax are similar with respect to morphological characters, coloration and body proportions, but differ considerably with respect to body size, fertility and longevity.The mitochondrial genes of both crayfish are similar, but some nuclear genomic features are markedly different. Both crayfish are eurytopic and have two major annual recruitment periods, but marbled crayfish show different population structure and higher invasiveness.Marbled crayfish occur in boreal to tropical habitats of Europe, Madagascar and Japan, but Procambarus fallax is confined to the subtropics and tropics of the southeastern USA.2 Laboratory experiments suggest reproductive isolation of both crayfish. The application of the Evolutionary Genetic Species Concept for asexuals to all available data supports raising marbled crayfish from "forma" to species rank. A determination key is provided to discriminate Procambarus virginalis, the first asexual decapod species, from its most likely parent species P. fallax. depth comparison of major aspects of life between marbled crayfish and its presumed parent species P. fallax, going beyond the state of information presented in Vogt et al. (2015) and Lyko (2017). Of particular importance is the variability of morphological characters, life history traits and genetic markers in both crayfish, that was not sufficiently considered in previous papers. Therefore, in this study we have compared morphology, life history, genetics, behaviour, ecology and biogeography between both crayfish, using numerous specimens from wild populations, laboratory colonies and museum collections. Additionally, we have performed a meta-analysis of our data and the literature data. For marbled crayfish, almost 250 publications are known, mainly based on laboratory studies (references in Faulkes, 2018;Vogt, 2018a). The number of publications on P. fallax is less than 50 and most of them are on its ecology (references in Hobbs, 1981;Hendrix et al., 2000;VanArman, 2011;van der Heiden & Dorn, 2017;Manteuffel et al., 2018).In the Results section we describe the similarities and differences between marbled crayfish and P. fallax with respect to morphological traits, coloration, body proportions, body size, fertil...

Epigenetic ecotypes in animals: persistent environmental adaptation in the absence of genetic variation

“…Despite this genetic uniformity, wild marbled crayfish populations showed considerable phenotypic differences to laboratory-raised populations with respect to growth, coloration, spination and body proportions (Vogt et al, 2018). For example, specimens from my laboratory reached maximum body lengths of only 9 cm and weights of 18 g, whereas their wild relatives in Lake Moosweiher, Germany, grew to ˜12 cm and 40 g (Figure 3C).…”

“…The marbled crayfish, Procambarus virginalis , is another good example of environmental adaptation by epigenetic phenotypes. This apomictic parthenogenetic all-female crayfish evolved from a single female of the Floridian slough crayfish, Procambarus fallax , by autotriploidization a few decades ago (Vogt et al, 2008(Vogt et al, , 2015(Vogt et al, , 2018(Vogt et al, , 2019Martin et al, 2010Martin et al, , 2016Vogt, 2020b;Legrand et al, 2021). It first appeared in the German aquarium trade in 1995 and was distributed from there across the world.…”

“…G, Germany (Maiakovska et al, 2021). (c) Maximum body sizes of laboratory raised and wild specimens from Lake Moosweiher (Germany), showing 30% bigger growth in the lake (from Vogt et al, 2018). (d) Chelipeds of specimens from the laboratory and Lake Moosweiher, showing bigger and sharper spines (arrows) in the wild specimen (from Vogt et al, 2018).…”

“…(c) Maximum body sizes of laboratory raised and wild specimens from Lake Moosweiher (Germany), showing 30% bigger growth in the lake (from Vogt et al, 2018). (d) Chelipeds of specimens from the laboratory and Lake Moosweiher, showing bigger and sharper spines (arrows) in the wild specimen (from Vogt et al, 2018). (e) Body proportions of marbled crayfish from the laboratory (L) and Lake Moosweiher (M) showing significant differences in total length/carapace length ratio (TL/CL) and carapace length/carapace width ratio (CL/CW).…”

“…Figure3Genetic, epigenetic and phenotypic differences between differently adapted populations of marbled crayfish, Procambarus virginalis . (a) Examples of strikingly different marbled crayfish habitats (fromVogt et al, 2018;Andriantsoa et al, 2019; Tönges et al, 2021a, b). (b) Genetic differences between representatives from different European populations as determined by whole-genome sequencing.…”