The clam genus Corbicula is an interesting model system to study the evolution of reproductive modes as it includes both sexual and asexual (androgenetic) lineages. While the sexual populations are restricted to the native Asian areas, the androgenetic lineages are widely distributed being also found in America and Europe where they form a major aquatic invasive pest. We investigated the genetic diversity of native and invasive Corbicula populations through a worldwide sampling. The use of mitochondrial and nuclear (microsatellite) markers revealed an extremely low diversity in the invasive populations with only four, undiversified, genetic lineages distributed across Europe and America. On the contrary, in the native populations, both sexual and androgenetic lineages exhibited much higher genetic diversity. Remarkably, the most abundant and widely distributed invasive forms, the so-called form A and form R found in America and Europe respectively, are fixed for the same single COI (cytochrome c oxydase subunit I) haplotype and same multilocus genotype. This suggests that form R, observed in Europe since the 1980s, derived directly from form A found in America since the 1920s. In addition, this form shares alleles with some Japanese populations, indicating a Japanese origin for this invasive lineage. Finally, our study suggests that few androgenetic Corbicula individuals successfully invaded the non-native range and then dispersed clonally. This is one striking case of genetic paradox raising the issue of invasive and evolutionary success of genetically undiversified populations.
BackgroundThe genus Corbicula is one of the most invasive groups of molluscs. It includes both sexual and androgenetic lineages. The present study re-assessed the different morphotypes and haplotypes of West European Corbicula in order to clarify their taxonomic identification and phylogenetic relationships with American and Asian Corbicula clams. We studied several populations from West European river basins (Meuse, Seine, Rhine and Rhône) through an "integrative taxonomy" approach. We combined morphology, partial mitochondrial COI and cyt b sequences and eleven microsatellite loci. Furthermore, we looked for discrepancies between mtDNA and nrDNA/morphology, indicative of androgenesis between lineages.ResultsThere are three Corbicula morphotypes in Western Europe associated to three mitochondrial lineages and three genotypes. Form R shares the same COI haplotype as the American form A and the Japanese C. leana. Form S and the American form C have the same haplotype, although their morphologies seem divergent. The European form Rlc belongs to the same mitochondrial lineage as both the American form B and the Asian C. fluminea.Interestingly, within each haplotype/genotype or lineage, no genetic diversity was found although their invasive success is high. Moreover, we detected rare mismatches between mtDNA and nrDNA/morphology, indicative of androgenesis and mitochondrial capture between form R and form S and therefore challenging the phylogenetic relatedness and the species status within this genus. The global phylogenetic analysis revealed that the sexual Corbicula lineages seem restricted to the native areas while their androgenetic relatives are widespread and highly invasive.ConclusionsWe clarified the discrepancies and incongruent results found in the literature about the European morphotypes of Corbicula and associated mitochondrial lineages. The three West European morphotypes belong to three distinct nuclear and mitochondrial lineages. However mitochondrial capture occurs in sympatric populations of forms R and S. The species status of the morphotypes therefore remains doubtful. Moreover the androgenetic lineages seem widely distributed compared to their sexual relatives, suggesting that androgenesis and invasive success may be linked in the genus Corbicula.
Among the asexual reproductive modes, androgenesis is probably one of the most astonishing and least studied mechanisms. In this 'paternal monopolization', the maternal nuclear genome fails to participate in zygote development and offspring are paternal nuclear clones. Obligate androgenesis is known in only a few organisms, including multiple species of clam in the genus Corbicula. Corbicula is a good system to review the evolutionary consequences of this 'all-male asexuality' because the cytological mechanisms of androgenetic reproduction have been described. In Corbicula, sperm are unreduced and, after fertilization, the maternal nuclear chromosomes are extruded as two polar bodies. Hermaphroditic lineages of Corbicula have a worldwide distribution and seem to reproduce through androgenesis, whereas their sexual relatives have restricted ranges. The invasive success of these androgenetic Corbicula lineages may be linked to their asexual mode of reproduction. We review the phenomenon of androgenesis, focusing on evolutionary perspectives, using the genus Corbicula as an exemplar system.
Genetic tools have been extremely useful to study the colonization history and dynamics of invasive species and infer source populations. In addition, understanding the distribution of genetic diversity of non-indigenous species is important to understand factors contributing to invasive success. Here, we used genetic markers to study the invasion history of the quagga mussel Dreissena rostriformis (Deshayes 1838). The invasion of North American and European watercourses by the quagga mussel is of major concern since this dreissenid mussel has widespread ecological and economic impacts in invaded regions. Through the use of mitochondrial (COI) and nuclear (microsatellites) markers and based on a large sampling, including both native and invasive ranges, we characterized the recent invasion of Western Europe by D. rostriformis. Scenario testing Bayesian analysis (approximate Bayesian computation methods) suggests that Western Europe was most probably invaded from the Pontic region via the southern corridor (Danube River, the Main-Danube Canal and the Main and Rhine rivers). Furthermore, pairwise F ST values suggest a second invasion to Western Europe from North America via trans-Atlantic shipping. The high genetic diversity and low differentiation among D. rostriformis populations suggest high propagule pressure and frequent exchanges between the Pontic region, Eastern North America and Western Europe. Our study concludes that multiple introductions and high propagule pressure have shaped the genetic composition of populations in Western Europe. The results provide valuable information for future management plans in order to control the spread of highly invasive aquatic species.
Occasional" sexuality occurs when a species combines clonal reproduction and genetic mixing. This strategy is predicted to combine the advantages of both asexuality and sexuality, but its actual consequences on the genetic diversity and species longevity are poorly understood. Androgenesis, a reproductive mode in which the offspring inherits its entire nuclear genome from the father, is often reported as a strictly clonal reproductive mode. Androgenesis is the predominant reproductive mode within the hermaphroditic, invasive lineages of the mollusk genus Corbicula. Their ability to reproduce clonally through androgenesis has been determinant in their invasive success, having colonized during the 20th century American and European freshwater systems, where they became notorious invaders with a widespread, global distribution. However, in androgenetic Corbicula clams, occasional genetic mixing between distinct lineages has also been observed when the sperm of one lineage fertilizes the oocyte of another one. Because of these occasional introgressions, the genetic relationships between Corbicula species remained unclear, and the biogeographic origins of the invasive androgenetic lineages have been challenging to identify. To address these issues, we analyzed the patterns of allele sharing for several nuclear and mitochondrial molecular markers among Corbicula individuals collected across both the native and invasive range. Our results show the occurrence of an allelic pool encompassing all Corbicula freshwater species worldwide, including sexual and androgenetic ones, which highlights the substantial genetic mixing within this genus. However, the differences in allele sharing patterns between invasive lineages, and the low diversity within each lineage, suggest recent, distinct biogeographic origins of invasive Corbicula androgenetic lineages. Finally, the polyploidy, high heterozygosity, and hybrid phenotypes and genotypes found in our study probably originated from hybridization events following egg parasitism between distinct Corbicula lineages. This extensive cross-lineage mixing found in Corbicula may generate nuclear diversity in an otherwise asexually reproducing species.
18Corbicula clams were introduced during the 20 th century into America and Europe, where they became 19 notoriously successful invaders with a widespread, global distribution. Their ability to reproduce clonally through 20 androgenesis ("all-male asexuality") has been determinant in their invasive success, with only four invasive clonal 21 lineages detected across Europe and America, one of which is very abundant and widespread on both continents. 22Due to their "all-male asexuality" and egg parasitism between distinct lineages, the evolutionary and geographic 23 origins of the invasive androgenetic lineages have been challenging to identify. We analyzed here the patterns of 24 allele sharing for different molecular markers among Corbicula individuals collected worldwide. We identify three 25 distinct genetic pools containing androgenetic Corbicula lineages. While one sexual Corbicula species forms a 26 distinct fourth genetic pool, the other sexual lineages cluster with the androgenetic ones based on shared alleles. 27One genetic pool contains most androgenetic lineages and sexual C. sandai from Lake Biwa in Japan, pointing to 28 this lake as a likely origin of androgenetic Corbicula lineages. Although three distinct biogeographic origins of 29Corbicula androgenetic lineages have been identified, their recent radiation and cross-lineage genetic mixing 30 hamper classical species delimitation within this clam genus. 31 32
The basket clam genus, Corbicula, commonly known as the Asian clam, has become one of the most internationally high-profile and widespread aquatic invasive species. This genus is now considered to comprise a polymorphic species complex. The international invasion of Corbicula is characterised by four lineages, each fixed for one morphotype, genotype and haplotype combination: the American form (A) and European round form (R), the American form (C) and European saddle from (S), American form B, form round light colour (Rlc) and an intermediate between forms R and S known as Int. We investigated the genetic and morphometric makeup of each Irish population in order to establish which invasive lineages were present so as to identify the number of introductions to Ireland. A combination of morphometric, mitochondrial cytochrome oxidase subunit I (mtCOI) gene analysis and microsatellite markers were used to determine the invasive form at each Irish site. All Irish Corbicula samples conformed morphometrically to the invasive form A/R. All mtCOI sequences retrieved for 25 Irish individuals were identical to the international A/R form, while microsatellite markers again showed a common clustering with the international A/R forms of Corbicula. The combined approach of morphometries, total genomic DNA and microsatellite markers indicate only one form of Corbicula invaded Ireland; the international A/R form.
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