The repeatable opportunity for selection differs between pre- and postcopulatory fitness components

In species with multiple mating, intense sexual selection may occur both before and after copulation. However, comparing the strength of pre‐ and postcopulatory selection is challenging, because (i) postcopulatory processes are generally difficult to observe and (ii) the often‐used opportunity for selection (I) metric contains both deterministic and stochastic components. Here, we quantified pre‐ and postcopulatory male fitness components of the simultaneously hermaphroditic flatworm, Macrostomum lignano. We did this by tracking fluorescent sperm-using transgenics-through the transparent body of sperm recipients, enabling to observe postcopulatory processes in vivo. Moreover, we sequentially exposed focal worms to three independent mating groups, and in each assessed their mating success, sperm‐transfer efficiency, sperm fertilizing efficiency, and partner fecundity. Based on these multiple measures, we could, for each fitness component, combine the variance (I) with the repeatability (R) in individual success to assess the amount of repeatable variance in individual success-a measure we call the repeatable opportunity for selection (IR). We found higher repeatable opportunity for selection in sperm‐transfer efficiency and sperm fertilizing efficiency compared to mating success, which clearly suggests that postcopulatory selection is stronger than precopulatory selection. Our study demonstrates that the opportunity for selection contains a repeatable deterministic component, which can be assessed and disentangled from the often large stochastic component, to provide a better estimate of the strength of selection

Social effects on fruit fly courtship song

LMO was supported by grants from the Swiss National Science Foundation (P2BSP3_158842 and P300PA_171516). NWB and MGR are supported by NERC, UK (NE/L011255/1 and grant NE/J020818/1, respectively).Courtship behavior in Drosophila has often been described as a classic innate behavioral repertoire, but more recently extensive plasticity has been described. In particular, prior exposure to acoustic signals of con‐ or heterspecific males can change courtship traits in both sexes that are liable to be important in reproductive isolation. However, it is unknown whether male courtship song itself is socially plastic. We examined courtship song plasticity of two species in the Drosophila melanogaster subgroup. Sexual isolation between the species is influenced by two male song traits, the interpulse interval (IPI) and sinesong frequency (SSF). Neither of these showed plasticity when males had prior experience of con‐ and heterospecific social partners. However, males of both species produced longer bursts of song during courtship when they were exposed to social partners (either con‐ or heterospecific) than when they were reared in isolation. D. melanogaster carrying mutations affecting short‐ or medium‐term memory showed a similar response to the social environment, not supporting a role for learning. Our results demonstrate that the amount of song a male produces during courtship is plastic depending on the social environment, which might reflect the advantage of being able to respond to variation in intrasexual competition, but that song structure itself is relatively inflexible, perhaps due to strong selection against hybridization.Publisher PDFPeer reviewe

Došašće/Advent Kratki oris i teološki uvod

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Indirect genetic effects and sexual conflicts: partner genotype influences multiple morphological and behavioural reproductive traits in a flatworm

The expression of an individual's phenotypic traits can be influenced by genes expressed in its social partners. Theoretical models predict that such indirect genetic effects (IGEs) on reproductive traits should play an important role in determining the evolutionary outcome of sexual conflict. However, empirical tests of (i) whether reproductive IGEs exist, (ii) how they vary among genotypes, and (iii) whether they are uniform for different types of reproductive traits are largely lacking. We addressed this in a series of experiments in the simultaneously hermaphroditic flatworm Macrostomum lignano. We found strong evidence for IGEs on both morphological and behavioral reproductive traits. Partner genotype had a significant impact on the testis size of focal individuals—varying up to 2.4-fold—suggesting that IGEs could mediate sexual conflicts that target the male sex function. We also found that time to first copulation was affected by a genotype × genotype interaction between mating partners, and that partner genotype affected the propensity to copulate and perform the postcopulatory suck behavior, which may mediate conflicts over the fate of received ejaculate components. These findings provide clear empirical evidence for IGEs on multiple behavioral and morphological reproductive traits, which suggests that the evolutionary dynamics of these traits could be altered by genes contained in the social environment.PostprintPeer reviewe

Sexual selection predicts species richness across the animal kingdom

Funding: Swiss National Science Foundation to T. J. (PA00P3-145375/1) and to L.M.-O. (P2BSP3_158842 and P300PA_171516).Our improving knowledge of the animal tree of life consistently demonstrates that some taxa diversify more rapidly than others, but what contributes to this variation remains poorly understood. An influential hypothesis proposes that selection arising from competition for mating partners plays a key role in promoting speciation. However, empirical evidence showing a link between proxies of this sexual selection and species richness is equivocal. Here, we collected standardized metrics of sexual selection for a broad range of animal taxa, and found that taxonomic families characterized by stronger sexual selection on males show relatively higher species richness. Thus, our data support the hypothesis that sexual selection elevates species richness. This could occur either by promoting speciation and/or by protecting species against extinction.PostprintPeer reviewe

Sperm competition-induced plasticity in the speed of spermatogenesis

Background: Sperm 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. Results: Here 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. Conclusions: Our 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

Sexual selection in a transparent worm : insights from fluorescent sperm

Sexual selection is a potent source of selection underlying the evolution of sexual dimorphism, reproductive strategies and mating systems. Although sexual selection was initially thought to occur exclusively at the pre-copulatory stage (e.g., contests among males, and female mate choice), it can also continue after copulation through sperm competition and/or cryptic female choice. However, the study of these post-copulatory processes remains challenging because they occur internally and so are often difficult to observe. During my PhD project, I used the simultaneously hermaphroditic flatworm Macrostomum lignano to study sexual selection, with a special focus on distinguishing the processes occurring at the pre- and post-copulatory stage of sexual selection. Mating is not necessarily a harmonious union, instead partners are expected to allocate their mating resources strategically over different mating opportunities to maximise their own fitness. My results suggests that virgin pairs have a greater mating propensity, presumably because they want to obtain sperm to fertilise their own eggs and have more sperm ready to give away. Moreover, in several species sperm donors have been shown to transfer accessory gland secretions along with sperm, which can manipulate the partners to increase donor's fitness. I speculate that this may also be the case in M. lignano as sperm recipients behave differently after mating with virgins, which likely transfer more accessory gland secretions. Progress in understanding post-copulatory processes of sexual selection greatly depends upon the development of techniques that facilitate the observation of internal processes. The unique opportunity to track sperm under competitive conditions inside the female reproductive tract in vivo has become possible thanks to a transgenic line ubiquitously expressing green fluorescent protein (GFP): fluorescent sperm in a transparent worm. I tested and validated the reliability of the GFP-techniques in M. lignano, from which I could take advantage to reach novel findings. Although sexual selection is recognised be composed of pre- and post-copulatory episodes of selection, few studies provide a quantitative understanding of the relative importance of the different episodes of selection. My results suggest that in M. lignano a large part of the variance observed in male reproductive success arises from two post-copulatory episodes of selection, sperm-transfer efficiency and sperm-fertilising efficiency. Moreover, individuals with bigger testis gain higher paternity share, presumably because they transfer more sperm per copulation. These two findings disagree with the view that sexual selection mainly arises from differences in mating success. Instead, the results suggest that in this study system the post-copulatory episodes of selection are very important, and that the success of these episodes likely depends upon the sperm production rate. Simultaneous hermaphrodites need to decide how they allocate their resources towards their own male and female sex functions. A fundamental theory is that this trade-off depends on the number of mating partners (i.e., mating group size). In particular, sex allocation theory predicts that individuals should allocate more energy towards their female function in small mating groups. When the mating group size increases, the intensity of sperm competition increases and so individuals are expected to increase their investment towards their male function. This is fully supported by my results, which represents the most direct test of this basic theory to date. In conclusion, the simultaneous hermaphrodite Macrostomum lignano is a powerful model organism to study sexual selection and sex allocation. My studies took advantage of several of its features to provide novel insights in fundamental topics such as the operation of sexual selection along episodes of selection and sex allocation in simultaneous hermaphrodites. Overall, my PhD works suggest that the post-copulatory episodes of sexual selection may be important agents of selection