TY - JOUR T1 - Mating behavior and reproductive morphology predict macroevolution of sex allocation in hermaphroditic flatworms JF - BMC Biology Y1 - 2022 DO - 10.1186/s12915-022-01234-1 A1 - Brand, Jeremias N. A1 - Harmon, Luke J. A1 - Schärer, Lukas SP - 35 AB -

Abstract Background Sex allocation is the distribution of resources to male or female reproduction. In hermaphrodites, this concerns an individual’s resource allocation to, for example, the production of male or female gametes. Macroevolutionary studies across hermaphroditic plants have revealed that the self-pollination rate and the pollination mode are strong predictors of sex allocation. Consequently, we expect similar factors such as the selfing rate and aspects of the reproductive biology, like the mating behaviour and the intensity of postcopulatory sexual selection, to predict sex allocation in hermaphroditic animals. However, comparative work on hermaphroditic animals is limited. Here, we study sex allocation in 120 species of the hermaphroditic free-living flatworm genus Macrostomum. We ask how hypodermic insemination, a convergently evolved mating behaviour where sperm are traumatically injected through the partner’s epidermis, affects the evolution of sex allocation. We also test the commonly-made assumption that investment into male and female reproduction should trade-off. Finally, we ask if morphological indicators of the intensity of postcopulatory sexual selection (female genital complexity, male copulatory organ length, and sperm length) can predict sex allocation. Results We find that the repeated evolution of hypodermic insemination predicts a more female-biased sex allocation (i.e., a relative shift towards female allocation). Moreover, transcriptome-based estimates of heterozygosity reveal reduced heterozygosity in hypodermically mating species, indicating that this mating behavior is linked to increased selfing or biparental inbreeding. Therefore, hypodermic insemination could represent a selfing syndrome. Furthermore, across the genus, allocation to male and female gametes is negatively related, and larger species have a more female-biased sex allocation. Finally, increased female genital complexity, longer sperm, and a longer male copulatory organ predict a more male-biased sex allocation. Conclusions Selfing syndromes have repeatedly originated in plants. Remarkably, this macroevolutionary pattern is replicated in Macrostomum flatworms and linked to repeated shifts in reproductive behavior. We also find a trade-off between male and female reproduction, a fundamental assumption of most theories of sex allocation. Beyond that, no theory predicts a more female-biased allocation in larger species, suggesting avenues for future work. Finally, morphological indicators of more intense postcopulatory sexual selection appear to predict more intense sperm competition.

VL - 20 UR - http://dx.doi.org/10.1186/s12915-022-01234-1 ER - TY - JOUR T1 - Frequent origins of traumatic insemination involve convergent shifts in sperm and genital morphology JF - Evolution Letters Y1 - 2021 DO - 10.1002/evl3.268 A1 - Brand, Jeremias N. A1 - Harmon, Luke J. A1 - Schärer, Lukas SP - 63 EP - 82 AB -

Traumatic insemination is a mating behavior during which the (sperm) donor uses a traumatic intromittent organ to inject an ejaculate through the epidermis of the (sperm) recipient, thereby frequently circumventing the female genitalia. Traumatic insemination occurs widely across animals, but the frequency of its evolution, the intermediate stages via which it originates, and the morphological changes that such shifts involve remain poorly understood. Based on observations in 145 species of the free-living flatworm genus Macrostomum, we identify at least nine independent evolutionary origins of traumatic insemination from reciprocal copulation, but no clear indication of reversals. These origins involve convergent shifts in multivariate morphospace of male and female reproductive traits, suggesting that traumatic insemination has a canalizing effect on morphology. We also observed sperm in both the sperm receiving organ and within the body tissue of two species. These species had intermediate trait values indicating that traumatic insemination evolves through initial internal wounding during copulation. Finally, signatures of male-female coevolution of genitalia across the genus indicate that sexual selection and sexual conflict drive the evolution of traumatic insemination, because it allows donors to bypass postcopulatory control mechanisms of recipients.

VL - 6 UR - http://dx.doi.org/10.1002/evl3.268 ER - TY - JOUR T1 - Large-scale phylogenomics of the genus Macrostomum (Platyhelminthes) reveals cryptic diversity and novel sexual traits JF - Molecular Phylogenetics and Evolution Y1 - 2022 DO - 10.1016/j.ympev.2021.107296 A1 - Brand, Jeremias N. A1 - Viktorin, Gudrun A1 - Wiberg, R. Axel W. A1 - Beisel, Christian A1 - Schärer, Lukas SP - 107296 AB -

Free-living flatworms of the genus Macrostomum are small and transparent animals, representing attractive study organisms for a broad range of topics in evolutionary, developmental, and molecular biology. The genus includes the model organism M. lignano for which extensive molecular resources are available, and recently there is a growing interest in extending work to additional species in the genus. These endeavours are currently hindered because, even though >200 Macrostomum species have been taxonomically described, molecular phylogenetic information and geographic sampling remain limited. We report on a global sampling campaign aimed at increasing taxon sampling and geographic representation of the genus. Specifically, we use extensive transcriptome and single-locus data to generate phylogenomic hypotheses including 145 species. Across different phylogenetic methods and alignments used, we identify several consistent clades, while their exact grouping is less clear, possibly due to a radiation early in Macrostomum evolution. Moreover, we uncover a large undescribed diversity, with 94 of the studied species likely being new to science, and we identify multiple novel morphological traits. Furthermore, we identify cryptic speciation in a taxonomically challenging assemblage of species, suggesting that the use of molecular markers is a prerequisite for future work, and we describe the distribution of putative synapomorphies and suggest taxonomic revisions based on our finding. Our large-scale phylogenomic dataset now provides a robust foundation for comparative analyses of morphological, behavioural and molecular evolution in this genus.

VL - 166 UR - http://dx.doi.org/10.1016/j.ympev.2021.107296 ER - TY - JOUR T1 - A phylogenetically informed search for an alternative Macrostomum model species, with notes on taxonomy, mating behavior, karyology, and genome size. JF - Journal of Zoological Systematics and Evolutionary Research Y1 - 2020 DO - 10.1111/jzs.12344 A1 - Schärer, Lukas A1 - Brand, Jeremias N. A1 - Singh, Pragya A1 - Zadesenets, Kira S. A1 - Stelzer, Claus-Peter A1 - Viktorin, Gudrun SP - 41–65 AB -

The free-living flatworm Macrostomum lignano is used as a model in a range of research fields—including ageing, bioadhesion, stem cells, and sexual selection—leading to the recent establishment of genome assemblies and transgenics. However, the Macrostomum community has run into a roadblock following the discovery of an unusual genome organization in M. lignano, which could impair the development of essential resources and tools. Briefly, M. lignano has undergone a whole-genome duplication, followed by rediploidisation into a 2n=8 karyotype (distinct from the canonical 2n=6 karyotype in the genus). Although this karyotype appears visually diploid, it is in fact a hidden tetraploid (with rarer 2n=9 and 2n=10 individuals being pentaploid and hexaploid, respectively). Here we report on a phylogenetically-informed search for close relatives of M. lignano, aimed at uncovering alternative Macrostomum models with the canonical karyotype and a simple genome organization. We taxonomically describe three new species: the first, Macrostomum janickei n. sp., is the closest known relative of M. lignano, and shares its derived genome organization; the second, Macrostomum mirumnovem n. sp., has an even more unusual genome organization, with a highly variable karyotype based on a 2n=9 base pattern; and the third, Macrostomum cliftonensis n. sp., does not only show the canonical 2n=6 karyotype, but also performs well under standard laboratory culture conditions and fulfils many other requirements. M. cliftonensis is a viable candidate for replacing M. lignano as the primary Macrostomum model, being outcrossing and having an estimated haploid genome size of only 231 Mbp.

VL - 58 ER -