Increase in multiple paternity across the reproductive lifespan in a sperm‐storing, hermaphroditic freshwater snail

Abstract

Polyandry is a common phenomenon and challenges the traditional view of stronger sexual selection in males than in females. In simultaneous hermaphrodites, the physical proximity of both sex functions was long thought to preclude the operation of sexual selection. Laboratory studies suggest that multiple mating and polyandry in hermaphrodites may actually be common, but data from natural populations are sparse. We therefore estimated the rate of multiple paternity and its seasonal variability in the annual, sperm-storing, simultaneously hermaphroditic freshwater snail Radix balthica for the entire duration of the reproductive lifespan. We also tested whether multiple paternity was associated with clutch size or embryonic development. To obtain these data, we measured and genotyped 60 field-collected egg clutches using nine highly polymorphic microsatellite markers. Overall, 50% of the clutches had multiple fathers, and both the frequency (20-93% of clutches) and magnitude of multiple paternity (mean 1.3-3.8 fathers per clutch) substantially increased over time, probably because of extensive sperm storage. Most multiply sired clutches (83%) had a dominant father, but neither clutch size nor the proportion of developed embryos per clutch was associated with levels of multiple paternity. Both the evident promiscuity and the frequent skew of paternity shares suggest that sexual selection may be an important evolutionary force in the study population.

Propensity for selfing varies within a population of hermaphroditic snails: coexistence of selfers, outcrossers and mixed-mating individuals

“…In Lake Zurich, Switzerland, it exhibits an annual life cycle with non-overlapping generations. Snails hatch from eggs in spring, reach sexual maturity in winter, reproduce from March to May, and then die [55]. During the single breeding season, individuals may copulate repeatedly in both sexual roles and lay hundreds of eggs in distinct egg clutches [55].…”

Why the architecture of environmental fluctuation matters for fitness

“…For example, Morris et al (2006) showed that, across five species of perennial plants in the USA, vital rates including seedling survival (equivalent to 𝑆𝑆 𝐽𝐽 here), survival at other stages, growth, germination, and seed production (equivalent to 𝑓𝑓 here) showed nonlinear change as a function of time since last hurricane or fire disturbance (disturbance phase). Similarly, Bürkli & Jokela (2017) showed that embryonic development success (early-stage juvenile survival) 13 of a freshwater snail changed nonlinearly across the species' reproductive season. The exact shape of vital rate response functions is another key point to be tailored for system-specific inquiry, whether with empirical measurements or as realistic assumptions built into models.…”

Selfing-outcrossing as a gradient, not a dichotomy: propensity for selfing varies within a population of hermaphroditic animals

“…In Lake Zurich, Switzerland, it is an annual with non-overlapping generations. Snails hatch from eggs in spring, reach sexual maturity in winter, reproduce from March to May, and then die (48). During the single breeding season, individuals may copulate repeatedly in both sexual roles and lay hundreds of eggs in distinct egg clutches (48).…”

“…Mating trials began in early May 2014 when F1 snails were 52.1 ± 1.0 weeks old and 38.7% had selfed in isolation. In the ancestral field population, breeding started in early March (48), and laboratory control snails had started to copulate several weeks earlier (see above). The experiment then continued for seven weeks, until mortality began to increase reflecting the snails' natural, annual life cycle.…”

“…We first ascertained how successfully 274 laboratory-reared, unmated snails selfed in isolation. We then assigned them to one of two mating treatments, simulating (i) a low population density and scarcity of mating opportunities, or (ii) conditions in the ancestral field population, where density was high and multiple paternity within egg clutches common (48). We recorded individual mating behaviour, the lifetime production of eggs in isolation (necessarily selfed) and thereafter (potentially outcrossed), and the proportion of developing eggs.…”