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Experimental evidence for reduced male allocation under selfing in a simultaneously hermaphroditic animal.

ABSTRACT: Self-fertilization is widespread among simultaneously hermaphroditic animals and plants, but is often only facultatively deployed under circumstances that constrain outcrossing. A central prediction of sex allocation (SA) theory is that because exclusive selfing reduces sperm or pollen competition to zero, this should favour extreme economy in resources channelled to the male sex function. We can therefore expect that organisms switching from outcrossing to selfing should reduce their male allocation. However, to date this prediction has received relatively little support in animal taxa, especially compared to plants. Here we show that isolated individuals (under enforced selfing conditions) have a less male-biased SA than do grouped conspecifics (under outcrossing conditions) in the preferentially outcrossing flatworm Macrostomum hystrix This shift arises from a reduced male allocation (testis area) in isolated individuals, although we did not find any evidence for a re-allocation of these resources to the female sex function (i.e. ovary area was unaffected by selfing/outcrossing conditions). Our results provide some of the clearest experimental evidence to date for reduced male allocation under selfing in simultaneously hermaphroditic animals, extending previous findings comparing SA between populations differing in selfing rates to the level of individual plasticity in gametogenesis.

SUBMITTER: Winkler L

PROVIDER: S-EPMC6227870 | biostudies-literature | 2018 Oct

REPOSITORIES: biostudies-literature

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Experimental evidence for reduced male allocation under selfing in a simultaneously hermaphroditic animal.

Winkler Lennart L Ramm Steven A SA

Biology letters 20181010 10

Self-fertilization is widespread among simultaneously hermaphroditic animals and plants, but is often only facultatively deployed under circumstances that constrain outcrossing. A central prediction of sex allocation (SA) theory is that because exclusive selfing reduces sperm or pollen competition to zero, this should favour extreme economy in resources channelled to the male sex function. We can therefore expect that organisms switching from outcrossing to selfing should reduce their male alloc ...[more]

PMID: 30305462

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Project description:BACKGROUND:Along with sperm, in many taxa ejaculates also contain large numbers of seminal fluid proteins (SFPs). SFPs and sperm are transferred to the mating partner, where they are thought to play key roles in mediating post-mating sexual selection. They modulate the partner's behavior and physiology in ways that influence the reproductive success of both partners, thus potentially leading to sexual conflict. Despite the presumed general functional and evolutionary significance of SFPs, their identification and characterization has to date focused on just a few animal groups, predominantly insects and mammals. Moreover, until now seminal fluid profiling has mainly focused on species with separate sexes. Here we report a comprehensive screen for putative SFPs in the simultaneously hermaphroditic flatworm Macrostomum lignano. RESULTS:Based on existing transcriptomic data, we selected 150 transcripts known to be (a) predominantly expressed in the tail region of the worms, where the seminal fluid-producing prostate gland cells are located, and (b) differentially expressed in social environments differing in sperm competition level, strongly implying that they represent a phenotypically plastic aspect of male reproductive allocation in this species. For these SFP candidates, we then performed whole-mount in situ hybridization (ISH) experiments to characterize tissue-specific expression. In total, we identified 98 transcripts that exhibited prostate-specific expression, 76 of which we found to be expressed exclusively in the prostate gland cells; additional sites of expression for the remaining 22 included the testis or other gland cells. Bioinformatics analyses of the prostate-limited candidates revealed that at least 64 are predicted to be secretory proteins, making these especially strong candidates to be SFPs that are transferred during copulation. CONCLUSIONS:Our study represents a first comprehensive analysis using a combination of transcriptomic and ISH screen data to identify SFPs based on transcript expression in seminal fluid-producing tissues. We thereby extend the range of taxa for which seminal fluid has been characterized to a flatworm species with a sequenced genome and for which several methods such as antibody staining, transgenesis and RNA interference have been established. Our data provide a basis for testing the functional and evolutionary significance of SFPs.

Dataset Information

Experimental evidence for reduced male allocation under selfing in a simultaneously hermaphroditic animal.

Publications

Experimental evidence for reduced male allocation under selfing in a simultaneously hermaphroditic animal.

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