Hardy exotics species in temperate zone: can "warm water" crayfish invaders establish regardless of low temperatures?
ABSTRACT: The spreading of new crayfish species poses a serious risk for freshwater ecosystems; because they are omnivores they influence more than one level in the trophic chain and they represent a significant part of the benthic biomass. Both the environmental change through global warming and the expansion of the pet trade increase the possibilities of their spreading. We investigated the potential of four "warm water" highly invasive crayfish species to overwinter in the temperate zone, so as to predict whether these species pose a risk for European freshwaters. We used 15 specimens of each of the following species: the red swamp crayfish (Procambarus clarkii), the marbled crayfish (Procambarus fallax f. virginalis), the yabby (Cherax destructor), and the redclaw (Cherax quadricarinatus). Specimens were acclimatized and kept for 6.5 months at temperatures simulating the winter temperature regime of European temperate zone lentic ecosystems. We conclude that the red swamp crayfish, marbled crayfish and yabby have the ability to withstand low winter temperatures relevant for lentic habitats in the European temperate zone, making them a serious invasive threat to freshwater ecosystems.
Project description:The 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.
Project description:BACKGROUND:The marbled crayfish (Procambarus virginalis) is a monoclonal, parthenogenetically reproducing freshwater crayfish species that has formed multiple stable populations worldwide. Madagascar hosts a particularly large and rapidly expanding colony of marbled crayfish in a unique environment characterized by a very high degree of ecological diversity. RESULTS:Here we provide a detailed characterization of five marbled crayfish populations in Madagascar and their habitats. Our data show that the animals can tolerate a wide range of ecological parameters, consistent with their invasive potential. While we detected marbled crayfish in sympatry with endemic crayfish species, we found no evidence for the transmission of the crayfish plague pathogen, a potentially devastating oomycete. Furthermore, our results also suggest that marbled crayfish are active predators of the freshwater snails that function as intermediate hosts for human schistosomiasis. Finally, we document fishing, farming and market sales of marbled crayfish in Madagascar. CONCLUSIONS:Our results provide a paradigm for the complex network of factors that promotes the invasive spread of marbled crayfish. The commercial value of the animals is likely to result in further anthropogenic distribution.
Project description:BACKGROUND:The parthenogenetic marbled crayfish (Procambarus virginalis) is a novel species that has rapidly invaded and colonized various different habitats. Adaptation to different environments appears to be independent of the selection of genetic variants, but epigenetic programming of the marbled crayfish genome remains to be understood. RESULTS:Here, we provide a comprehensive analysis of DNA methylation in marbled crayfish. Whole-genome bisulfite sequencing of multiple replicates and different tissues revealed a methylation pattern that is characterized by gene body methylation of housekeeping genes. Interestingly, this pattern was largely tissue invariant, suggesting a function that is unrelated to cell fate specification. Indeed, integrative analysis of DNA methylation, chromatin accessibility and mRNA expression patterns revealed that gene body methylation correlated with limited chromatin accessibility and stable gene expression, while low-methylated genes often resided in chromatin with higher accessibility and showed increased expression variation. Interestingly, marbled crayfish also showed reduced gene body methylation and higher gene expression variability when compared with their noninvasive mother species, Procambarus fallax. CONCLUSIONS:Our results provide novel insights into invertebrate gene body methylation and its potential role in adaptive gene regulation.
Project description:The marbled crayfish (Procambarus virginalis) represents a very recently evolved parthenogenetic freshwater crayfish species that has invaded diverse habitats in Europe and in Madagascar. However, population genetic analyses have been hindered by the homogeneous genetic structure of the population and the lack of suitable tools for data analysis. We have used whole-genome sequencing to characterize reference specimens from various known wild populations. In parallel, we established a whole-genome sequencing data analysis pipeline for the population genetic analysis of nearly monoclonal genomes. Our results provide evidence for systematic genetic differences between geographically separated populations and illustrate the emerging differentiation of the marbled crayfish genome. We also used mark-recapture population size estimation in combination with genetic data to model the growth pattern of marbled crayfish populations. Our findings uncover evolutionary dynamics in the marbled crayfish genome over a very short evolutionary timescale and identify the rapid growth of marbled crayfish populations as an important factor for ecological monitoring.
Project description:The negative environmental and economic impacts of many invasive species are well known. However, given the increased homogenization of global biota, and the difficulty of eradicating species once established, a balanced approach to considering the impacts of invasive species is needed. The marbled crayfish (Procambarus virginalis) is a parthenogenetic freshwater crayfish that was first observed in Madagascar around 2005 and has spread rapidly. We present the results of a socio-economic survey (n = 385) in three regions of Madagascar that vary in terms of when the marbled crayfish first arrived. Respondents generally considered marbled crayfish to have a negative impact on rice agriculture and fishing, however the animals were seen as making a positive contribution to household economy and food security. Regression modeling showed that respondents in regions with longer experience of marbled crayfish have more positive perceptions. Unsurprisingly, considering the perception that crayfish negatively impact rice agriculture, those not involved in crayfish harvesting and trading had more negative views towards the crayfish than those involved in crayfish-related activities. Food preference ranking and market surveys revealed the acceptance of marbled crayfish as a cheap source of animal protein; a clear positive in a country with widespread malnutrition. While data on biodiversity impacts of the marbled crayfish invasion in Madagascar are still completely lacking, this study provides insight into the socio-economic impacts of the dramatic spread of this unique invasive species. "Biby kely tsy fantam-piaviana, mahavelona fianakaviana" (a small animal coming from who knows where which supports the needs of the family). Government worker Analamanga, Madagascar.
Project description:Freshwater biodiversity is globally threatened by various factors while severe weather events like long-term droughts may be substantially devastating. In order to remain in contact with the water or stay in a sufficiently humid environment at drying localities, the ability to withstand desiccation by dwelling in the hyporheic zone, particularly through vertical burrowing is crucial. We assessed the ability of three European native and five non-native crayfish as models to survive and construct vertical burrows in a humid sandy-clayey substrate under a simulated one-week drought. Three native species (Astacus astacus, A. leptodactylus, and Austropotamobius torrentium) suffered extensive mortalities. Survival of non-native species was substantially higher while all specimens of Cherax destructor and Procambarus clarkii survived. The native species and Pacifastacus leniusculus exhibited no ability to construct vertical burrows. Procambarus fallax f. virginalis and P. clarkii constructed bigger and deeper burrows than C. destructor and Orconectes limosus. In the context of predicted weather fluctuations, the ability to withstand desiccation through constructing vertical burrows into the hyporheic zone under drought conditions might play a significant role in the success of particular crayfish species, as well as a wide range of further hyporheic-dwelling aquatic organisms in general.
Project description:Self-cloning is quite rare in shrimp, lobsters, crayfish and crabs. Here we report the discovery of four natural clones of red swamp crayfish (Procambarus clarkii), each containing 2-6 genetically identical individuals, during the genotyping of 120 individuals with five microsatellites. The four clones were heterozygote at most of the five microsatellite loci. Phylogenetic analysis using microsatellite genotypes suggests recent origin of the four clones. Sequencing a part of the mitochondrial gene Cox I confirmed that the four clones were from the species Procambarus clarkii.
Project description:Male sexual differentiation in crustaceans is controlled by the androgenic gland (AG), a unique male endocrine organ that, in decapods, is located at the base of the 5th pereiopod. In these animals, the insulin-like androgenic gland hormone (IAG) is the major factor secreted from the AG to induce masculinization and maintain male characteristics. It has, however, recently been proposed that this hormone also plays a role in growth and ovarian development in females. In this study, we tested such a possibility by searching for the IAG gene in the marbled crayfish, a parthenogenetic animal that reproduces asexually to form an all-female genetic clone. Based on the phylogenetic relationship between the marbled crayfish and Procambarus fallax, a gonochoristic species of the same North American Cambaridae family, we searched for the IAG gene in the marbled crayfish and then fully sequenced it. The open reading frame of the gene was found to be completely identical in the two species, and their introns shared over 94% identity. It was also found that, in addition to its expression at the base of the 5th pereiopod and in the testes of male P. fallax crayfish, IAG was expressed in the muscle tissue of P. fallax males and females and even of the parthenogenetic marbled crayfish. These findings provide new insight into possible functions of IAG, in addition to its role as a masculinization-inducing factor, and also constitute the basis for a discussion of the evolutionary relationship between the above two species.
Project description:Biological invasions by nonindigenous species can have negative effects on economies and ecosystems. To limit this impact, current research on biological invasions uses functional traits to facilitate a mechanistic understanding of theoretical and applied questions. Here we aimed to assess the role of functional traits in the progression of crayfish species through different stages of invasion and determine the traits associated with invasive success. A dataset of thirteen functional traits of 15 species currently occurring or available for sale in the Netherlands was evaluated. Six of these crayfish appeared invasive. Important traits distinguishing successful from unsuccessful invaders were a temperate climate in the native range, a medium to high egg count and producing more than one egg clutch per year. The most successful invaders had different functional trait combinations: Procambarus clarkii has a higher reproductive output, can migrate over longer distances and possesses a higher aggression level; Faxonius limosus is adapted to a colder climate, can reproduce parthenogetically and has broader environmental tolerances. Using a suit of functional traits to analyse invasive potential can help risk management and prevention. For example, based on our data Procambarus virginalis is predicted to become the next successful invasive crayfish in the Netherlands.
Project description:Red swamp crayfish (Procambarus clarkii) breeding is an important economic mainstay in Hubei province, China. However, information on the gut microbiota of the red swamp crayfish is limited. To address this issue, the effect of developmental stage, diet (fermented or non-fermented feed), and geographical location on the gut microbiota composition in the crayfish was studied via high-throughput 16S rRNA gene sequencing. The results revealed that the dominant phyla in the gut of the crayfish were Proteobacteria, Bacteroidetes,Firmicutes, Tenericutes, and RsaHF231. The alpha diversity showed a declining trend during development, and a highly comparable gut microbiota clustering was identified in a development-dependent manner. The results also revealed that development, followed by diet, is a better key driver for crayfish gut microbiota patterns than geographical location. Notably, the relative abundance of Bacteroidetes was significantly higher in the gut of the crayfish fed with fermented feed than those fed with non-fermented feed, suggesting the fermented feed can be important for the functions (e.g., polysaccharide degradation) of the gut microbiota. In summary, our results revealed the factors shaping gut microbiota of the crayfish and the importance of the fermented feed in crayfish breeding.