Search bioRxiv⌕ Search

bioRxiv · 10.1101/2021.03.28.437366

Large-scale phylogenomics of the genus Macrostomum (Platyhelminthes) reveals cryptic diversity and novel sexual traits

Abstract

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 possible 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.

Source connections

Explore related subjects

Keep this discovery

Explore connections, maps & timelines

BibTeXRIS

Brand, J., Viktorin, G., Wiberg, R. A. W., Beisel, C., Schaerer, L.. 2021-03-29. Large-scale phylogenomics of the genus Macrostomum (Platyhelminthes) reveals cryptic diversity and novel sexual traits. https://doi.org/10.1101/2021.03.28.437366

Cite the original work for its findings. Save a collection to share your selection of sources.

KEEP EXPLORING

Related preprints

Global homeostatic forces shape the composition of a hyperdiverse tropical insect fauna

Despite comprising the bulk of terrestrial biodiversity, we know surprisingly little about insect faunas, particularly in the tropics. Here, we characterize the insect fauna of Madagascar, a global biodiversity hotspot, based on extensive DNA metabarcoding of Malaise trap and leaf litter samples. We estimate that the fauna comprises at least 250,000 species, only 5% of which are currently recorded. The ecological and taxonomic composition is surprisingly similar to that of temperate forests. We show that this is likely caused by global homeostatic forces shaping net diversification rates after colonization of Madagascar rather than by the composition of colonizing lineages. Features differing from temperate forests include the dearth of parasitoids and richness of beetles. Understanding the forces shaping these patterns is key in sustainable management of tropical insect faunas.

evolutionary biology↗

Do divergent mitochondrial backgrounds alter the fate of nuclear alleles during hybridization and admixture?

Hybridization brings together genetic variation from different populations or species into admixed genomes. As selection sorts this variation, the fate of each allele is determined by its fitness effect in the new hybrid genomic background. Because mitochondrial genes coevolve with the nuclear genome, they may be especially sensitive to foreign nuclear backgrounds, making them potential "hot-spots" for hybrid incompatibilities. Here, we test whether selection against mitonuclear incompatibilities drives repeatable hybridization outcomes. Specifically, we experimentally evolved three sets of five populations of hybrid Drosophila melanogaster, each carrying the same nuclear chromosomes but paired with one of three increasingly divergent mitochondrial DNA backgrounds. We hypothesized that accumulated incompatibilities would result in different patterns of nuclear admixture among mitochondrial backgrounds. To test this, we tracked nuclear allele frequencies in all 15 populations by whole-genome sequencing at intermediate time points. After 25 generations, we observed that rapid genomic evolution produced a strikingly parallel mosaic of both nuclear ancestries, independent of mitochondrial background. Contrary to our hypothesis, we found no evidence that mitochondrial background1 shaped nuclear admixture, even for interspecific combinations. These results suggest that in species with large effective population sizes, efficient purifying selection limits the accumulation of mitonuclear incompatibilities, allowing selection on nuclear alleles to promote repeatable ancestry sorting immediately following hybridization.

evolutionary biology↗

Body size cascades from Neodiprion sawfly hosts to Perilampid parasitoids: An investigation of sequential divergence

Ecological speciation drives diversity in plant-eating insect systems, but it may also generate parallel specialization in parasitoid associates in a cascading effect of "sequential divergence." However, sequential divergence has never been successfully identified in parasitoids of externally feeding insects. To address this gap, we consider the Pinus-Neodiprion-Perilampus neodiprioni system, where plant-associated, externally feeding Neodiprion demonstrate ecological divergence, as supported by body size as a magic trait in sympatric species. It seems possible that this body size differentiation may cascade to Neodiprion's parasitoids via sequential divergence. Therefore, we asked, "Does P. neodiprioni exhibit host-specific divergence in body size that parallels patterns in Neodiprion hosts?" Further, "Does P. neodiprioni exhibit host-related variation in the abdominal region or sexually dimorphic features, supporting reproductive barriers?" Using by-catch samples, we measured body size of P. neodiprioni, reared from Neodiprion lecontei and Neodiprion pinetum hosts. We analyzed body size variation as predicted by host species, parasitoid sex, host sex, host cocoon size, latitude, and their interactions. In addition, we used mixed models to analyze the effects of parasitoid sex and Neodiprion host on three size-based facial features. We found that P. neodiprioni demonstrates host-associated body size variation that mirrors size differences in their Neodiprion hosts. In addition, host-associated size variation occurs in the abdominal region and two sexually dimorphic characters of P. neodiprioni, supporting possible reproductive isolation. Together, these patterns suggest that host magic traits may drive not only within-species ecological divergence, but they can facilitate parasitoids' subsequent morphological differentiation and possible sequential divergence.

evolutionary biology↗