Sperm competition affects sex allocation but not sperm morphology in a flatworm

Janicke, Tim; Schärer, Lukas

doi:10.1007/s00265-010-0951-y

Cited by 29 publications

(45 citation statements)

References 55 publications

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“…To document sperm morphology, we recovered worms from squeeze preparations, amputated the tail plate (64), and ruptured it by placing it on a microscope slide in 1-2 μL of liquid and covering it with a coverslip. Fully formed sperm emerged from the ruptured seminal vesicle and were documented (65). Because sperm are sensitive to low osmotic pressure, we added small amounts of diluted seawater for freshwater species to prevent osmotic damage to the sperm (artifacts thereof sometimes are reported as bona fide sperm morphology).…”

Section: Methodsmentioning

confidence: 99%

Mating behavior and the evolution of sperm design

Schärer

Littlewood

Waeschenbach

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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118

312

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Sperm are the most diverse of all animal cell types, and much of the diversity in sperm design is thought to reflect adaptations to the highly variable conditions under which sperm function and compete to achieve fertilization. Recent work has shown that these conditions often evolve rapidly as a consequence of multiple mating, suggesting a role for sexual selection and sexual conflict in the evolution of sperm design. However, very little of the striking diversity in sperm design is understood functionally, particularly in internally fertilizing organisms. We use phylogenetic comparative analyses covering 16 species of the hermaphroditic flatworm genus Macrostomum to show that a complex sperm design is associated with reciprocal mating and that this complexity is lost secondarily when hypodermic insemination-sperm injection through the epidermis-evolves. Specifically, the complex sperm design, which includes stiff lateral bristles, is likely a male persistence trait associated with sexual conflicts over the fate of received ejaculates and linked to female resistance traits, namely an intriguing postcopulatory sucking behavior and a thickened epithelium of the sperm-receiving organ. Our results suggest that the interactions between sperm donor, sperm, and sperm recipient can change drastically when hypodermic insemination evolves, involving convergent evolution of a needle-like copulatory organ, a simpler sperm design, and a simpler female genital morphology. Our study documents that a shift in the mating behavior may alter fundamentally the conditions under which sperm compete and thereby lead to a drastic change in sperm design.Platyhelminthes | sexually antagonistic coevolution | simultaneous hermaphrodite | sperm morphology | traumatic insemination P arker's (1-3) far-reaching extension of Darwin's (4) narrow focus on precopulatory mating interactions highlighted that sexual selection continues to operate after mating partners have agreed to mate and that considering postcopulatory sexual selection therefore is crucial to understand the evolution of many reproductive traits (5, 6). This insight has led to extensive research in evolutionary biology that focused on understanding the biology of sperm (7), the most diverse of all animal cell types (8,9). From this research emerged an apparent consensus that the diversity in sperm design-the strikingly variable ways of constructing a sperm-reflects the highly variable physiological and morphological environments in which sperm have to survive, function, and compete for fertilization (5,(10)(11)(12)(13)(14). Moreover, recent studies have documented clearly that these environments can evolve rapidly, probably because of coevolutionary interactions linked to multiple mating and the resulting sexual selection and sexual conflicts (15-21). However, the bewildering diversity in sperm design is poorly understood at the functional level, particularly in internally fertilizing organisms (9,12,22). A recent review on the evolution of sperm morphological diversity concluded...

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Section: Methodsmentioning

confidence: 99%

Mating behavior and the evolution of sperm design

Schärer

Littlewood

Waeschenbach

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

118

312

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“…For example, in the flatworm Macrostomum lignano worms raised in larger social groups have larger testes (Schärer & Ladurner, 2003;Brauer, Schärer & Michiels, 2007), a heightened testicular cell proliferation activity (Schärer et al, 2004), and produce more sperm (Schärer & Vizoso, 2007). Furthermore, given that sperm production in large social groups is higher per unit testis size, other sperm production parameters, such as the speed of spermatogenesis or the size of the produced sperm (but see Janicke & Schärer, 2010), may also vary in response to social conditions (Schärer & Vizoso, 2007).…”

Section: (3) Sperm Production Plasticitymentioning

confidence: 99%

“…In intraspecific studies a recurring pattern is for sperm morphometry to differ substantially among individuals but relatively little within individuals, both in species with separate sexes (Ward, 1998;Morrow & Gage, 2001) and in hermaphrodites (Minoretti & Baur, 2006;Janicke & Schärer, 2010). To elucidate the origin of these patterns comparative analyses in different bird groups have suggested that betweenindividual variation in sperm size is most pronounced in species subject to low levels of sperm competition, probably due to relaxed selection on an optimal sperm morphometry and so too presumably on other aspects of spermatogenesis (Birkhead et al, 2005;Calhim, Immler & Birkhead, 2007;Kleven et al, 2008;Lüpold, Linz & Birkhead, 2009a).…”

Section: (2) Variation and Plasticity In Sperm Morphology Within Speciesmentioning

confidence: 99%

The evolutionary ecology of testicular function: size isn't everything

Ramm

Schärer

2014

Biological Reviews

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Larger testes are considered the quintessential adaptation to sperm competition. However, the strong focus on testis size in evolutionary research risks ignoring other potentially adaptive features of testicular function, many of which will also be shaped by post-mating sexual selection. Here we advocate a more integrated research programme that simultaneously takes into account the developmental machinery of spermatogenesis and the various selection pressures that act on this machinery and its products. The testis is a complex organ, and so we begin by outlining how we can think about the evolution of testicular function both in terms of the composition and spatial organisation of the testis ('testicular histology'), as well as in terms of the logical organisation of cell division during spermatogenesis ('testicular architecture'). We then apply these concepts to ask which aspects of testicular function we can expect to be shaped by post-mating sexual selection. We first assess the impact of selection on those traits most strongly associated with sperm competition, namely the number and kind of sperm produced. A broad range of studies now support our contention that post-mating sexual selection affects many aspects of testicular function besides gross testis size, for example, to maximise spermatogenic efficiency or to enable the production of particular sperm morphologies. We then broaden our focus to ask how testicular function is affected by fluctuation in sperm demand. Such fluctuation can occur over an individual's lifetime (for example due to seasonality in reproduction) and may select for particular types of testicular histology and architecture depending on the particular reproductive ecology of the species in question. Fluctuation in sperm demand also occurs over evolutionary time, due to shifts in the mating system, and this may have various consequences for testicular function, for example on rates of proliferation-induced mutation and for dealing with intragenomic conflict. We end by suggesting additional approaches that could be applied to study testicular function, and conclude that simultaneously considering the machinery, products and scheduling of spermatogenesis will be crucial as we seek to understand more fully the evolution of this most fundamental of male reproductive traits.

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“…Crean and Marshall (Crean and Marshall, 2008) showed that males alter the phenotype of their gametes in response to increases in the risk of sperm competition, and that this gamete plasticity resulted in higher fertilisation success when sperm concentrations were high. Gamete plasticity in response to sperm competition is not Environmentally induced (co)variance in sperm and offspring phenotypes as a source of epigenetic effects Dustin J. Marshall* universal, however: Janicke and Schärer (Janicke and Schärer, 2010) found no evidence for changes in sperm morphology in response to sperm competition in flatworms, despite major changes in sex allocation between treatments. Nevertheless, gamete plasticity in response to sperm competition represents an important source of variation in sperm phenotype in a range of species and therefore a potential source of non-genetic effects.…”

Section: Reviewmentioning

confidence: 99%

Environmentally induced (co)variance in sperm and offspring phenotypes as a source of epigenetic effects

Marshall

2015

Journal of Experimental Biology

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Traditionally, it has been assumed that sperm are a vehicle for genes and nothing more. As such, the only source of variance in offspring phenotype via the paternal line has been genetic effects. More recently, however, it has been shown that the phenotype or environment of fathers can affect the phenotype of offspring, challenging traditional theory with implications for evolution, ecology and human in vitro fertilisation. Here, I review sources of non-genetic variation in the sperm phenotype and evidence for co-variation between sperm and offspring phenotypes. I distinguish between two environmental sources of variation in sperm phenotype: the prerelease environment and the post-release environment. Pre-release, sperm phenotypes can vary within species according to male phenotype (e.g. body size) and according to local conditions such as the threat of sperm competition. Post-release, the physicochemical conditions that sperm experience, either when freely spawned or when released into the female reproductive tract, can further filter or modify sperm phenotypes. I find evidence that both pre-and post-release sperm environments can affect offspring phenotype; fertilisation is not a new beginning -rather, the experiences of sperm with the father and upon release can drive variation in the phenotype of the offspring. Interestingly, there was some evidence for co-variation between the stress resistance of sperm and the stress resistance of offspring, though more studies are needed to determine whether such effects are widespread. Overall, it appears that environmentally induced covariation between sperm and offspring phenotypes is non-negligible and further work is needed to determine their prevalence and strength.

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Sperm competition affects sex allocation but not sperm morphology in a flatworm

Cited by 29 publications

References 55 publications

Mating behavior and the evolution of sperm design

Mating behavior and the evolution of sperm design

The evolutionary ecology of testicular function: size isn't everything

Environmentally induced (co)variance in sperm and offspring phenotypes as a source of epigenetic effects

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