Seasonal effects on egg production and level of paternity in a natural population of a simultaneous hermaphrodite snail

Abstract

In a seasonal environment, the suitable time window for females to reproduce is restricted by both environmental conditions and the availability of males. In simultaneous hermaphrodites, which are female and male at the same time, selection on a trait that is solely beneficial for one sexual function cannot occur independently. Therefore, it is assumed that the optimal time window for reproduction is a compromise between the two sexual functions in simultaneous hermaphrodites, mediated by environmental conditions. We examined seasonal patterns of reproduction and the resulting paternity in a natural population of the simultaneously hermaphroditic land snail Arianta arbustorum. Adult and premature individuals (snails in a short protandric phase) were collected on four occasions over the entire active season. The snails were allowed to deposit eggs after which we assessed the level of paternity in their hatched offspring. Individuals mated throughout the reproductive season, whereas egg production – the major task of the female function – was restricted to the first half of the season. Snails collected in autumn were allowed to hibernate under laboratory conditions. As a result, we found that premature individuals began to mate late in the reproductive season, but did not start to produce eggs before emerging from hibernation. Our results demonstrate a temporal shift of reproductive activities; the egg production and oviposition occur mainly in the first half of the season, while sperm production and mating occur over the entire season. In subadult and adult snails, sperm obtained from several partners in the second part of the reproductive season are stored during hibernation for the fertilization of eggs in the successive years. These results extend our understanding of the influence of both natural and sexual selection on reproductive strategies in hermaphrodites.

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

“…Only a few studies have examined temporal trends in multiple paternity in hermaphrodites, all of them using laboratory‐laid egg clutches. Neither in the marine snail Aplysia californica (Angeloni et al., ) nor in A. arbustorum (Janssen & Baur, ), there was any evidence for such trends, although in A. arbustorum one study found more multiple paternity among adult than subadult snails (Kupfernagel & Baur, ). Also in gonochorists, data on within‐season variation in multiple paternity are very scarce.…”

“…For example, in the freshwater snail Lymnaea stagnalis, 59% of clutches were multiply sired and clutches had a minimum number of 1.8 fathers on average (Nakadera et al., ). In Physa acuta , another freshwater snail, clutches had a mean of 3.8 fathers (Henry et al., ), and in the terrestrial snail Ariana arbustorum 68.3% to 100% of clutches were multiply sired, and clutches had 4.0–6.1 fathers on average (Janssen & Baur, ; Kupfernagel & Baur, ; Kupfernagel et al., ). Interestingly, our estimates of multiple paternity rates are approximately in the same range as these laboratory‐based estimates.…”

“…Many hermaphroditic animals have been shown to mate multiply, mostly under laboratory conditions (e.g., Jordaens, Dillen, & Backeljau, ), but in a few cases also in the field (e.g., Anthes, Putz, & Michiels, ). Moreover, in the majority of studied hermaphroditic species, multiple paternity within broods or clutches, providing a minimum estimate of the degree of polyandry in a population (Anthes, Häderer, Michiels, & Janicke, ; Dunn & Lifjeld, ; Griffith, ; Uller & Olsson, ), turned out to be common (e.g., Angeloni, Bradbury, & Burton, ; Henry, Bousset, Sourrouille, & Jarne, ; Janssen & Baur, ; Lorenzi, Schleicherová, & Sella, ; Pongratz & Michiels, ; Proestou, Goldsmith, & Twombly, ). Finally, in two species of simultaneously hermaphroditic freshwater snails, sexual selection has been measured explicitly and proved to be quite similar in strength and direction to corresponding values of gonochoric species (Anthes et al., ; Pélissié, Jarne, & David, ).…”

“…Numbers of matings and the degree of multiple paternity have often been assessed using laboratory mating trials, which not only alter the conditions under which copulations and reproduction take place, but also predefine the number and identity of available mating partners (e.g., Evanno, Madec, & Arnaud, ; Garefalaki, Triantafyllidis, Abatzopoulos, & Staikou, ; Koene, Montagne‐Wajer, Roelofs, & Ter Maat, ; Kupfernagel & Baur, ; Lorenzi et al., ; Pongratz & Michiels, ). In other studies, presumably inseminated adults have been collected in the field and then kept in isolation, and rates of multiple paternity have been measured among the progeny produced in the laboratory (e.g., Angeloni et al., ; Henry et al., ; Janssen & Baur, ; Nakadera, Mariën, Van Straalen, & Koene, ). Although making fewer assumptions than the laboratory mating trials, also these studies assume that multiple paternity rates measured in the laboratory reflect those in the natural field populations.…”

“…Both inter‐ and intraspecific variation in multiple paternity may thus be substantial in hermaphrodites, and obtaining more data from natural populations is essential. In addition, the frequency and extent of multiple paternity in a population may change during an individual's lifetime, something that has never been studied in a free‐living hermaphrodite (but see Angeloni et al., ; Kupfernagel & Baur, ; Janssen & Baur, for studies using laboratory‐produced progenies of field‐collected adults). The occurrence of temporal changes in multiple paternity is likely because many hermaphroditic species have, just like numerous gonochorists, the ability to store, mix and potentially choose between received sperm from earlier matings (e.g., Cain, ; Madsen, Waithaka Thiongo, & Ouma, ; Nakadera, Blom, & Koene, ; Vianey‐Liaud, Nassi, Lancastre, & Dupouy, ).…”