Patterns of distribution, population genetics and ecological requirements of field-occurring resistant and susceptible Pseudosuccinea columella snails to Fasciola hepatica in Cuba

Abstract

Pseudosuccinea columella snails transmit the trematode Fasciola hepatica, but in Cuba, six naturally occurring populations successfully resist parasite infection. Here, we present an updated distribution of P. columella in Cuba; 68 positive sites with the earliest records more abundant in west-central Cuba and with east-central populations generally corresponding to the newest samples. No records were found farther east. The IPA site reported 10.5% prevalence of F. hepatica-infected snails. Population genetics, studied through microsatellites, showed low allelic and multilocus genotypic richness (MLGT), mainly in susceptible populations, strong deviations from panmixia and high self-fertilization rates. Susceptible individuals were grouped in one major cluster containing the majority of MLGT, and two independent clusters grouped the MLGT of resistant individuals from western and central populations, respectively. From these, we propose that several introductions of P. columella occurred in Cuba, primarily in the west, with the early arrivals deriving on the resistant populations. A more recent introduction of susceptible P. columella carrying MLGT T and Y may have occurred, where the latter spread quickly through the island and possibly increase the risk of parasite transmission in Cuba since all snails naturally infected with F. hepatica were carriers of the MLGT Y. Interestingly, even though resistant populations are highly diverse and are likely the oldest within Cuba, they are only found in six localities characterized by soft (total hardness, TH = 6.3 ± 1.03°d) and slightly acidic (pH = 6.2 ± 0.12) waters with low richness in snail species (3.2 ± 1.02). This tendency was also observed in a two-year follow-up ecological study that was conducted on a farm where both phenotypes occurred in sympatry; colonization events by resistant over susceptible snails coincided with a reduction in the pH and TH of the water. A comparison of life traits in susceptible and resistant isolates reared at two different pH/TH conditions (5.9/4°d or 7.8/14°d) showed that low pH/TH negatively affects P. columella, irrespective of the phenotype. However, evidence of higher tolerance (higher survival, life expectancy, egg viability) to such conditions was observed in resistant isolates. Finally, we speculate that the limited distribution of resistant populations might be related to a better exploitation of sites that are less suitable to snails (thus, with lower competition), rather than to a differential ecological restriction to specific environmental conditions from susceptible P. columella.

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

“…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).…”

Geography and ecology of invasive Pseudosuccinea columella (Gastropoda: Lymnaeidae) and implications in the transmission of Fasciola species (Digenea: Fasciolidae) – a review

“…Pseudosuccinea columella is thought to have originated from Central America, the Caribbean and the southern part of North America (Mas-Coma et al, 2005), and this review has shown that this species has been successfully introduced and established in other continents with varying environmental and ecological conditions. The results from this review showed that in addition to its native regions (Dar et al, 2014;Martin et al, 2016;Lounnas et al, 2017;Alba et al, 2018;Vignoles et al, 2018;Carolus et al, 2019), P. columella has been documented in Africa, Europe, South America (Martin et al, 2016;Lounnas et al, 2017;Alba et al, 2018) and Oceania (Martin et al, 2016;Lounnas et al, 2017;Alba et al, 2018;Vignoles et al, 2018;Alba et al, 2019b). The results further indicate that from these four newly invaded continents, this invasive freshwater snail has been reported in 19 countries, but is now well established and widely distributed in Africa and South America, and is least distributed in Oceania (Lounnas et al, 2017).…”

Schistosoma mansoni Vector Snails in Antigua and Montserrat, with Snail-Related Considerations Pertinent to a Declaration of Elimination of Human Schistosomiasis

“…Physa acuta was collected from one locality, and Physa marmorata was collected at 10 different localities, and a few were positive for either strigeid or xiphidiocercaria infections. Pseudosuccinea columella , a known snail host for Fasciola hepatica in Cuba, 25 was collected at four different localities, and none were shedding trematodes.…”