Genomic evidence for hybridization, mitochondrial capture and cryptic invasions in the Chinese mitten crab Eriocheir sinensis (Crustacea: Decapoda: Brachyura: Varunidae)

Abstract Enhanced genetic diversity arising from interspecific hybridisation and from multiple introductions from different source populations has played a major role in the evolution of invasive traits in introduced populations. Across Europe, mitochondrial haplotypes associated with the Japanese mitten crab Eriocheir japonica have been discovered in populations of the Chinese mitten crab Eriocheir sinensis, one of Europe’s highest priority aquatic invasive non-native species, suggesting a possible cryptic invasion of a second Eriocheir species. Analysis of the nuclear genomes of mitten crabs from one of these populations based on single nucleotide polymorphisms (SNPs) obtained through genotyping by sequencing, combined with landmark analysis of carapace morphology indicates that the crabs resemble E. sinensis in their morphology and nuclear genomic background, regardless of whether they carry an E. sinensis or E. japonica mitochondrial haplotype. This suggests interspecific introgression of mitochondrial DNA originating in the Japanese mitten crab Eriocheir japonica at some point in the population’s history, either in its native range or following introduction to Europe. A discrete cluster of SNP genotypes is associated with the E. japonica mitochondrial haplotype in samples from 2015 but not from 2020, suggesting an intraspecific cryptic invasion of genetically distinct mitten crabs into a previously established population, followed by interbreeding. Genetically diverse and novel hybrid biological invaders require particularly careful monitoring since they are likely to display enhanced evolutionary potential, with their life cycles and ecology possibly diverging from that of ancestral populations in their native range. In addition, mitochondrial environmental DNA and DNA barcoding of mitochondrial markers are increasingly relied upon to detect and identify aquatic non-native species. The potential for mitochondrial introgression between species to confuse these methods must be considered.