Abstract
BackgroundSperm competition between rival ejaculates over the fertilization of ova typically selects for the production of large numbers of sperm. An obvious way to increase sperm production is to increase testis size, and most empirical work has focussed on this parameter. Adaptive plasticity in sperm production rate could also arise due to variation in the speed with which each spermatozoon is produced, but whether animals can respond to relevant environmental conditions by modulating the kinetics of spermatogenesis in this way has not been experimentally investigated.ResultsHere we demonstrate that the simultaneously hermaphroditic flatworm Macrostomum lignano exhibits substantial plasticity in the speed of spermatogenesis, depending on the social context: worms raised under higher levels of sperm competition produce sperm faster.ConclusionsOur findings overturn the prevailing view that the speed of spermatogenesis is a static property of a genotype, and demonstrate the profound impact that social environmental conditions can exert upon a key developmental process. We thus identify, to our knowledge, a novel mechanism through which sperm production rate is maximised under sperm competition.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0629-9) contains supplementary material, which is available to authorized users.
Highlights
Sperm competition between rival ejaculates over the fertilization of ova typically selects for the production of large numbers of sperm
We here establish for the first time, to our knowledge, that there is social environmentally-induced plasticity in the speed of spermatogenesis: worms raised under higher levels of sperm competition produce sperm faster
Testis size plasticity We performed an experiment to manipulate the levels of sperm competition by keeping worms (n = 720) in two different social group sizes (‘pairs’ and ‘octets’), followed by labelling and immunocytochemical tracking of proliferating testicular germ cells, to a) confirm the expected phenotypic plasticity in testis size usually observed in these worms in response to altered social and mating group size (e.g. [32, 34]), and b) test the main hypothesis of this study that worms kept in larger social groups increase the speed of spermatogenesis
Summary
Sperm competition between rival ejaculates over the fertilization of ova typically selects for the production of large numbers of sperm. Whilst only a single sperm is required to fertilize each ovum, the number of sperm produced by males (or in the case of simultaneous hermaphrodites, the male sex function) usually greatly exceeds the number of ova produced by females (or the female sex function) This apparent profligacy likely evolved as a direct consequence of disruptive selection on gamete size and number during the evolution of anisogamy, and is maintained because of sperm competition, which occurs when the ejaculates from two or more sperm donors compete over fertilization and which creates an evolutionary arms race between conspecific rivals over sperm production [1,2,3,4]. These include the histological and logical organisation of spermatogenesis as well as its kinetics, and accumulating evidence suggests that these sources of variation warrant further investigation from a sperm competition
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