Occurrence, costs and heritability of delayed selfing in a free‐living flatworm

Abstract

Evolutionary theory predicts that in the absence of outcrossing opportunities, simultaneously hermaphroditic organisms should eventually switch to self-fertilization as a form of reproductive assurance. Here, we report the existence of facultative self-fertilization in the free-living flatworm Macrostomum hystrix, a species in which outcrossing occurs via hypodermic insemination of sperm into the parenchyma of the mating partner. First, we show that isolated individuals significantly delay the onset of reproduction compared with individuals with outcrossing opportunities ('delayed selfing') as predicted by theory. Second, consistent with the idea of M. hystrix being a preferential outcrosser under natural conditions, we report likely costs of selfing manifested via reduced hatchling production and offspring survival. Third, we demonstrate that selfing propensity has a genetic basis in this species, with a heritability estimated at 0.43 ± 0.11. Variation in selfing propensity could arise due to differing costs of inbreeding among families; despite marked inter-family variation in apparent costs of inbreeding, we found no evidence for such a link. Alternatively, selfing propensity might differ across families because of heritable variation in reproductive traits that determine the likelihood of selfing. We speculate that adaptations to hypodermic insemination under outcrossing, most notably a highly modified copulatory stylet (male copulatory organ) and reduced sperm complexity, could also facilitate facultative selfing in this species.

Self-fertilization, sex allocation and spermatogenesis kinetics in the hypodermically-inseminating flatworm Macrostomum pusillum

“…These adaptations to hypodermic insemination are likely also of assistance to the ability to self-fertilize (Ramm et al, 2015). Our study represents the first demonstration that M. pusillum can self-fertilize, rendering it the second species in the Macrostomum clade known to perform this type of mating, the other being M. hystrix (Ramm et al, 2012). How exactly M. pusillum engages in self-fertilization is currently unknown, but a recent study in the morphologically similar congener M. hystrix revealed that this occurs by hypodermic self-insemination into its body and head regions, presumably because the own anterior part of the body is more easily reached by the copulatory organ located in the tail (Ramm et al, 2015).…”

“…Theory predicts an optimal waiting time before commencing self-fertilization, related to the intensity of inbreeding depression in the progeny, the ability to re-allocate reproductive resources to later fecundity and the probability of finding a partner versus dying as the individual ages (Tsitrone et al, 2003a). Empirical evidence for delayed selfing in line with these predictions comes from a variety of hermaphroditic organisms, including plants (Kalisz et al, 1999;Qu et al, 2007), freshwater snails (Tsitrone et al, 2003b;Auld & Henkel, 2014; but see Escobar et al, 2007), cestodes (Schjørring, 2004, but see Schärer & Wedekind, 1999 and the flatworm M. hystrix, which delays reproduction for up to 50% of the average age at first outcrossing, when forced to self (Ramm et al, 2012).…”

“…However, in the extended absence of mating opportunities, isolated M. hystrix individuals can switch to self-fertilization (Ramm et al, 2012) by hypodermic self-insemination (Ramm et al, 2015), despite significant inbreeding depression in the progeny (Ramm et al, 2012).…”

“…Second, from an ecological perspective, selfing can act as a reproductive assurance mechanism when mate availability is low (Darwin, 1876;Jain, 1976), as is the case for many organisms (e.g. Jarne et al, 1991;Kalisz et al, 1999;Tsitrone et al, 2003b;Schjørring, 2004;Noel et al, 2016), including the hermaphroditic flatworm Macrostomum hystrix (Ramm et al, 2012).…”

“…predominantly outcrossing with high inbreeding depression (e.g. Tsitrone et al, 2003b;Ramm et al, 2012), a strategy that is adaptive because it maintains population heterozygosity at high levels. However, mixed mating systems with intermediate selfing rates, although rare, occur as well; their existence has been argued to depend strongly on ecological circumstances (Goodwillie et al, 2005;Jarne and Auld, 2006).…”