Self‐fertilization, long‐distance flash invasion and biogeography shape the population structure of Pseudosuccinea columella at the worldwide scale

Abstract

Population genetic studies are efficient for inferring the invasion history based on a comparison of native and invasive populations, especially when conducted at species scale. An expected outcome in invasive populations is variability loss, and this is especially true in self-fertilizing species. We here focus on the self-fertilizing Pseudosuccinea columella, an invasive hermaphroditic freshwater snail that has greatly expanded its geographic distribution and that acts as intermediate host of Fasciola hepatica, the causative agent of human and veterinary fasciolosis. We evaluated the distribution of genetic diversity at the largest geographic scale analysed to date in this species by surveying 80 populations collected during 16 years from 14 countries, using eight nuclear microsatellites and two mitochondrial genes. As expected, populations from North America, the putative origin area, were strongly structured by selfing and history and harboured much more genetic variability than invasive populations. We found high selfing rates (when it was possible to infer it), none-to-low genetic variability and strong population structure in most invasive populations. Strikingly, we found a unique genotype/haplotype in populations from eight invaded regions sampled all over the world. Moreover, snail populations resistant to infection by the parasite are genetically distinct from susceptible populations. Our results are compatible with repeated introductions in South America and flash worldwide invasion by this unique genotype/haplotype. Our study illustrates the population genetic consequences of biological invasion in a highly selfing species at very large geographic scale. We discuss how such a large-scale flash invasion may affect the spread of fasciolosis.

The Evolutionary Interplay between Adaptation and Self-Fertilization

“…Recent invasions can also be caused by human-mediated long-distance dispersal. A unique genotype of the freshwater snail Pseudosuccinea columella was found in eight worldwide regions, which could have spread due to the global trade of aquarium-related plants and seawater [58]. However, for these two examples we still do not know whether the colonizing genotypes possessed exceptional invasive ability, or were simply the luckiest ones.…”

Reviewing Fasciola hepatica transmission in the West Indies and novel perceptions from experimental infections of sympatric vs. allopatric snail/fluke combinations

“…Given that snails and/or parasites may migrate (by means of natural or human mediated introduction), more susceptible/infective genotypes could be introduced in the future shaping transmission atterns. Invasive genotypes of the lymnaeid host P. columella introduced worldwide are supposed to have facilitated the spread of F. hepatica in many regions due to a lack of genetic diversity that may counteract infection (Lounnas et al, 2017). In Cuba, for example, the same effect has been observed and the only infected natural populations of P. columella carried a widespread genotype particularly present in monomorphic populations (Alba et al 2019).…”

Fasciola hepatica-Pseudosuccinea columella interaction: effect of increasing parasite doses, successive exposures and geographical origin on the infection outcome of susceptible and naturally-resistant snails from Cuba

“…Pseudosuccinea columella (Say, 1817), considered native from North America [ 3 ], can be also cited among the intermediate host species of F. hepatica in South America and the Caribbean [ 4 – 6 ]. In addition, it is a globally invasive freshwater snail that has been largely introduced out of its native range [ 3 ] with reports of established populations from Europe [ 7 ], Africa [ 8 ], Australia [ 9 ] and the Pacific islands [ 10 , 11 ]. The global spread of some invasive genotypes of P. columella might complicate the epidemiological scenario of fasciolosis transmission [ 3 ].…”