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Hypodermic self-insemination as a reproductive assurance strategy.

ABSTRACT: Self-fertilization occurs in a broad range of hermaphroditic plants and animals, and is often thought to evolve as a reproductive assurance strategy under ecological conditions that disfavour or prevent outcrossing. Nevertheless,selfing ability is far from ubiquitous among hermaphrodites, and may be constrained in taxa where the male and female gametes of the same individual cannot easily meet. Here, we report an extraordinary selfing mechanism in one such species, the free-living flatworm Macrostomum hystrix. To test the hypothesis that adaptations to hypodermic insemination of the mating partner under outcrossing also facilitate selfing, we experimentally manipulated the social environment of these transparent flatworms and then observed the spatial distribution of received sperm in vivo. We find that this distribution differs radically between conditions allowing or preventing outcrossing, implying that isolated individuals use their needle-like stylet (male copulatory organ) to inject own sperm into their anterior body region, including into their own head, from where they then apparently migrate to the site of (self-)fertilization. Conferring the ability to self could thus be an additional consequence of hypodermic insemination, a widespread fertilization mode that is especially prevalent among simultaneously hermaphroditic animals and probably evolves due to sexual conflict over the transfer and subsequent fate of sperm.

SUBMITTER: Ramm SA

PROVIDER: S-EPMC4528547 | biostudies-literature | 2015 Jul

REPOSITORIES: biostudies-literature

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Hypodermic self-insemination as a reproductive assurance strategy.

Ramm Steven A SA Schlatter Aline A Poirier Maude M Schärer Lukas L

Proceedings. Biological sciences 20150701 1811

Self-fertilization occurs in a broad range of hermaphroditic plants and animals, and is often thought to evolve as a reproductive assurance strategy under ecological conditions that disfavour or prevent outcrossing. Nevertheless,selfing ability is far from ubiquitous among hermaphrodites, and may be constrained in taxa where the male and female gametes of the same individual cannot easily meet. Here, we report an extraordinary selfing mechanism in one such species, the free-living flatworm Macro ...[more]

PMID: 26136446

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Project description:Background and aimsIn animal-pollinated plants, direct and indirect selection for large and small flowers in predominantly outcrossing and selfing species, respectively, is a common consequence of pollen limitation (PL). However, many hermaphroditic species show a mixed-mating system known as delayed selfing, which provides reproductive assurance (RA) only when outcrossing is not realized. Although RA is expected to reduce pollinator-mediated selection towards larger flowers, the consequences of delayed selfing for selection on flower size in mixed-mating species remain overlooked. We investigated whether RA weakens selection on flower size in Tuberaria guttata, a mixed-mating annual herb.MethodsWe related pollinator visitation rates to flower size and measured seed production in emasculated, hand cross-pollinated and intact (control) flowers in three natural populations. For each population, we estimated variation in PL and RA across individuals differing in flower size and phenotypic selection on this trait.Key resultsPollinator visitation increased and RA decreased with flower size in all populations. Increasing RA diminished but did not fully alleviate PL, because of early-acting inbreeding depression. In the least-visited and most pollen-limited population, RA increased seed production by >200 %, intensely counteracting the strong pollinator-mediated selection for larger corollas. In the most-visited population, however, RA increased seed production by an average of only 9 %. This population exhibited the largest fraction of individuals that showed a decrease in seed production due to selfing and the weakest pollinator-mediated selection on flower size.ConclusionsThe results suggest that the balance between the extent of RA and outcrossing contributes to determine flower size in mixed-mating systems. Pollinator-mediated selection favours larger flowers by increasing outcrossed seeds, but the benefits of RA greatly lessen this effect, especially under severe conditions of pollen limitation. Our findings also indicate that a mixed-mating system can represent an 'evolutionary trap' under an adequate pollinator supply.

Project description:Spatiotemporal segregation is often explained by the risk for offspring predation or by differences in physiology, predation risk vulnerability or competitive abilities related to size dimorphism. Most large carnivores are size dimorphic and offspring predation is often intraspecific and related to nonparental infanticide (NPI). NPI can be a foraging strategy, a strategy to reduce competition, or a male reproductive strategy. Spatiotemporal segregation is widespread among large carnivores, but its nature remains poorly understood. We evaluated three hypotheses to explain spatiotemporal segregation in the brown bear, a size-dimorphic large carnivore in which NPI is common; the 'NPI - foraging/competition hypothesis', i.e. NPI as a foraging strategy or a strategy to reduce competition, the 'NPI - sexual selection hypothesis', i.e. infanticide as a male reproductive strategy and the 'body size hypothesis', i.e. body-size-related differences in physiology, predation risk vulnerability or competitive ability causes spatiotemporal segregation. To test these hypotheses, we quantified spatiotemporal segregation among adult males, lone adult females and females with cubs-of-the-year, based on GPS-relocation data (2006-2010) and resource selection functions in a Scandinavian population. We found that spatiotemporal segregation was strongest between females with cubs-of-the-year and adult males during the mating season. During the mating season, females with cubs-of-the-year selected their resources, in contrast to adult males, in less rugged landscapes in relative close proximity to certain human-related variables, and in more open habitat types. After the mating season, females with cubs-of-the-year markedly shifted their resource selection towards a pattern more similar to that of their conspecifics. No strong spatiotemporal segregation was apparent between females with cubs-of-the-year and conspecifics during the mating and the postmating season. The 'NPI - sexual selection hypothesis' best explained spatiotemporal segregation in our study system. We suggest that females with cubs-of-the-year alter their resource selection to avoid infanticidal males. In species exhibiting NPI as a male reproductive strategy, female avoidance of infanticidal males is probably more common than observed or reported, and may come with a fitness cost if females trade safety for optimal resources.

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Hypodermic self-insemination as a reproductive assurance strategy.

Publications

Hypodermic self-insemination as a reproductive assurance strategy.

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