Substantial genetic mixing among sexual and androgenetic lineages within the clam genus Corbicula

Abstract

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.

Salinity appears to be the main factor shaping spatial COI diversity of Corbicula lineages within the Chinese Yangtze River Basin

“…The biological species concept, which defines species as units that exhibit barriers to reproduction, is widely used to delimit taxonomical units. The different reproductive strategies found in Corbicula (androgenetic hermaphrodite, sexual dioecism, cross‐fertilization and self‐fertilization (Gomes et al, 2016; Peñarrubia et al, 2017; Pigneur, Etoundi, et al, 2014)), as well as possible hybridization between distinct lineages (Hedtke et al, 2008; Lee et al, 2005; Pigneur, Etoundi, et al, 2014; Vastrade et al, 2022), make species delimitation in general using the biological species concept problematic in this genus. Genetic lineages defined using the COI marker, as in the present study, can identify distinct mitochondrial lineages within the genus Corbicula as evidenced by other studies (e.g.…”

“…Control and management of invasive species are highlighted as a priority for biodiversity conservation (Coughlan et al, 2020; Guareschi et al, 2021). Corbicula lineages A/R and B are abundant and widely distributed in native and invaded regions (Gomes et al, 2016; Park & Kim, 2003; Peñarrubia et al, 2017; Pigneur, Etoundi, et al, 2014), and their peculiar reproductive mode (including androgenesis, self‐ and cross‐fertilization) may be one of the main reasons for their invasive capacities in freshwater ecosystems (Gomes et al, 2016; Kraemer et al, 1986; Lee et al, 2005; Vastrade et al, 2022). Importantly, our findings here revealed that these two lineages had a wide tolerance to salinity being able to colonize from estuary to inland rivers and lakes, increasing their invasion potential in different water systems.…”

“…All sequences from Chinese Corbicula individuals were aligned using the plugin ClustalW Alignment (Thompson et al, 1994) in Geneious (Gap Open Cost = 100 and Gap Extend Cost = 10: R11, Biomatters Ltd.). Moreover, the COI sequences of the four identified invasive lineages in Europe and America (Hedtke et al, 2008; Park & Kim, 2003; Pigneur et al, 2011; Pigneur, Etoundi, et al, 2014; Siripattrawan et al, 2000; Vastrade et al, 2022), being FW5 (form A/R, NCBI ID: AF196268) (Siripattrawan et al, 2000), FW1 (form B, AF196269) (Siripattrawan et al, 2000), FW4 (form Rlc, AF269096) (Renard et al, 2000) and FW17 (form C/S, AF269095) (Renard et al, 2000), were added to the alignment and phylogenetic reconstruction to compare native Chinese and invasive Corbicula specimens using COI . Furthermore, Corbicula spp .…”

“…In recent years, with the development of sequencing methods, molecular markers have been employed to solve taxonomical difficulties (e.g. Bespalaya et al, 2018; Haponski & Ó Foighil, 2019; Vastrade et al, 2022). Two Corbicula mitochondrial lineages are now considered to be widely distributed within Asian freshwater environments using COI , forms A/R and B (Park & Kim, 2003; Pigneur, Etoundi, et al, 2014; Wang et al, 2014).…”

“…Two Corbicula mitochondrial lineages are now considered to be widely distributed within Asian freshwater environments using COI , forms A/R and B (Park & Kim, 2003; Pigneur, Etoundi, et al, 2014; Wang et al, 2014). However, discrepancies remain between genetic and morphological identifications (Lee et al, 2005; Siripattrawan et al, 2000), as well as between nuclear and mitochondrial markers (Hedtke et al, 2008; Lee et al, 2005; Peñarrubia et al, 2017; Pfenninger et al, 2002; Vastrade et al, 2022). The taxonomical identification of Corbicula also remains difficult because of their androgenetic mode of reproduction and polyploidy.…”