Search bioRxiv⌕ Search

Biology subjects

Brand, J. N.

Publications and source records attributed to Brand, J. N..

7 recordsLinked to original sources

Stepwise emergence of recombination suppression precedes fissiparous asexuality in the planarian Schmidtea mediterranea

A central paradox in evolutionary biology is the rarity of asexual reproduction, which is often attributed to developmental constraints and long-term costs. Yet, fissiparous asexuality--where animals split and regenerate--is widespread among planarians, hinting at genomic features predisposing them to asexuality. We investigated the genomic underpinnings and evolutionary consequences of asexuality in the planarian Schmidtea mediterranea, which exists as both obligately fissiparous and sexual strains. We generated a haplotype-phased genome assembly of the asexual strain and collected population genomic data from laboratory and wild populations to uncover extensive heterozygous chromosomal rearrangements affecting all chromosomes. We show that these rearrangements arose in a sexually reproducing ancestor without directly disrupting reproductive genes but instead progressively suppressing recombination across the genome. The asexual genome exhibits minimal deleterious mutation accumulation, indicating a low cost of asexuality. Population-genomic data show this strain lacks any detectable sexual reproduction and originated recently (0.17-0.4 Ma), but the young age is insufficient to explain the low mutational burden. Instead, planarians may be able to exploit the lack of a single-cell bottleneck in fissiparous reproduction to mitigate the costs of asexuality. Altogether, our results support a model in which stepwise recombination suppression due to structural rearrangements eroded the benefits of sex and enabled the emergence of fissiparous asexuality in S. mediterranea.

evolutionary biology↗

An integrative taxonomic approach reveals unexplored diversity in Croatian planarians

BackgroundFreshwater ecosystems are among the most endangered habitats on Earth, with approximately one-fourth of aquatic species at risk of extinction. Effective conservation efforts require comprehensive monitoring and accurate species identification, including often overlooked groups. DNA barcoding promises rapid and accessible species identification but requires the availability of "universal" primer pairs and robust, taxonomically curated reference libraries. Planarian flatworms are one such group for which these resources are currently lacking, even though they are common constituents of freshwater ecosystems worldwide. As a result, the true extent of planarian diversity remains underappreciated in many areas. ResultsMotivated by the highly skewed representation of planarian diversity in current GenBank records of the barcoding gene mitochondrial cytochrome c oxidase subunit I (COI), we optimised existing barcoding primers and tested them on planarians collected in a species-rich but, so far, poorly surveyed region of Croatia. Using an integrative approach combining the new primers, traditional taxonomy and karyology, we generated new taxonomically curated COI barcode sequences for European dugesiids, dendrocoelids and planariids, which, in the case of the latter two groups, represent a substantial increase of the number of entries for those families. Our efforts resulted in several significant findings, including the description of a new pigmented Dendrocoelum species, Dendrocoelum pigmentatum sp. nov, the discovery of two highly differentiated haplotypic clades in Schmidtea lugubris, and the rediscovery of Polycladodes alba in Croatia after a century. ConclusionsOverall, our work extends the utility of DNA barcoding for species-level identification of planarians to previously inaccessible groups. Additionally, it integrates Croatia as an underexplored but species-rich region into the endeavour to systematically describe the planarian fauna of Europe. The expansion of a known number of Croatian planarian species from eight to sixteen and the discovery of a new, large planarian species in continental Europe, Dendrocoelum pigmentatum, demonstrate the effectiveness of our integrative approach. Overall, our work highlights the underappreciated diversity of planarians, even in continental Europe and supports practical conservation efforts to preserve aquatic biodiversity.

zoology↗

A comparative analysis of planarian genomes reveals regulatory conservation in the face of rapid structural divergence

The planarian Schmidtea mediterranea can regenerate its entire body from small tissue fragments and is studied as regeneration model species. The assembly and functional analysis of planarian genomes has proven challenging due its high A/T content (70% A/T), repetitive nature, and limited transferability of routine laboratory protocols due to their divergent biochemistry. Only few and often fragmented genome assemblies are currently available, and open challenges include the provision of well-annotated chromosome-scale reference assemblies of the model species and other planarians for a comparative genome evolution perspective. Here we report a haplotype-phased, chromosome-scale genome assembly and high-quality gene annotations of the sexual S2 strain of S. mediterranea and provide putative regulatory region annotations via optimized ATAC-seq and ChIP-seq protocols. To additionally leverage sequence conservation for regulatory element annotations, we generated chromosome-scale genome assemblies and chromatin accessibility data for the three closest relatives of S. mediterranea: S. polychroa, S. nova, and S. lugubris. We find substantial divergence in protein-coding sequences and regulatory regions, yet reveal remarkable conservation in ChIP-mark bearing open chromatin regions identified as promoters and enhancers in S. mediterranea. The resulting high-confidence set of evolutionary conserved enhancers and promoters provides a valuable resource for the analysis of gene regulatory circuits and their evolution within the taxon. In addition, our four chromosome-scale genome assemblies provide a first comparative perspective on planarian genome evolution. Our analyses reveal frequent retrotransposon-associated chromosomal inversions and inter-chromosomal translocations that lead to a degradation of synteny across the genus. Interestingly, we further find independent and near-complete losses of the ancestral metazoan synteny across Schmidtea and two other flatworm groups, indicating that platyhelminth genomes largely evolve without syntenic constraints. Our work provides valuable genome resources for the planarian research community and sets a foundation for the comparative genomics of planarians. We reveal a contrast between the fast structural evolution of planarian genomes and the conservation of their regulatory elements, suggesting a unique genome evolution in flatworms where gene positioning may not be essential.

genomics↗

Probing the evolutionary dynamics of whole-body regeneration within planarian flatworms

Why some animals can regenerate while many others cannot remains a fascinating question. Even amongst planarian flatworms, well-known for their ability to regenerate complete animals from small body fragments, species exist that have restricted regeneration abilities or are entirely regeneration incompetent. Towards the goal of probing the evolutionary dynamics of regeneration, we have assembled a diverse live collection of planarian species from around the world. The combined quantification of species-specific head regeneration abilities and comprehensive transcriptome-based phylogeny reconstructions reveals multiple independent transitions between robust whole-body regeneration and restricted regeneration in the freshwater species. Our demonstration that the RNAi-mediated inhibition of canonical Wnt signalling can nevertheless bypass all experimentally tractable head regeneration defects in the current collection indicates that the pathway may represent a hot spot in the evolution of planarian regeneration defects. Combined with our finding that Wnt signalling has multiple roles in the reproductive system of the model species S. mediterranea, this raises the possibility of a trade-off between egg-laying and asexual reproduction by fission/regeneration as a driver of regenerative trait evolution. Although initial quantitative comparisons of Wnt signalling levels, reproductive investment, and regenerative abilities across the collection confirm some of the models predictions, they also highlight the diversification of molecular mechanisms amongst the divergent planarian lineages. Overall, our study establishes a framework for the mechanistic evolution of regenerative abilities and planarians as model taxon for comparative regeneration research.

evolutionary biology↗

Evolution and co-evolution of the suck behaviour, a postcopulatory female resistance trait that manipulates received ejaculate

Sexual conflicts over the post-mating fate of received ejaculate can favour traits in one sex that are costly to the other. Reciprocally mating hermaphrodites face unique challenges as they mate simultaneously in both the male and female role, potentially leading to receipt of unwanted ejaculate. Reciprocal mating can then give rise to postcopulatory female resistance traits that allow manipulation of received ejaculate. A putative example is the suck behaviour, observed in the flatworm genus Macrostomum. It involves the sperm recipient placing its pharynx over its own female genital opening and appearing to suck, likely removing received ejaculate after mating. The genus also contains hypodermically-inseminating species that presumably exhibit unilateral mating and have not been observed to suck. Here, we examine the evolution of the suck behaviour in Macrostomum, aiming to document the mating behaviour in 64 species. First, we provide videographic evidence that ejaculate is indeed removed during the suck behaviour in a reciprocally mating species, Macrostomum hamatum. Next, we show evolutionary positive correlations between the presence, duration and frequency of reciprocal mating behaviour and the suck behaviour, providing clear evidence that the suck behaviour co-evolves with reciprocal mating behaviour. Finally, we show an association between reproductive behaviour and reproductive morphology, suggesting that reproductive morphology can be used for inferring the behavioural mating strategy of a species. Together our study demonstrates sexual antagonistic coevolution leading to the evolution of a postcopulatory behavioural trait that functions as a female counter-adaptation allowing individuals to gain control over received ejaculate in a hermaphroditic sexual system.

evolutionary biology↗

Faster rates of molecular sequence evolution in reproduction-related genes and in species with hypodermic sperm morphologies

Sexual selection drives the evolution of many striking behaviours and morphologies, and should leave signatures of selection at loci underlying these phenotypes. However, while loci thought to be under sexual selection often evolve rapidly, few studies have contrasted rates of molecular sequence evolution at such loci across lineages with different sexual selection contexts. Furthermore, work has focused on separate sexed animals, neglecting alternative sexual systems. We investigate rates of molecular sequence evolution in hermaphroditic flatworms of the genus Macrostomum. Specifically, we compare species that exhibit contrasting sperm morphologies, strongly associated with multiple convergent shifts in the mating strategy, reflecting different sexual selection contexts. Species donating and receiving sperm in every mating have sperm with bristles, likely to prevent sperm removal. Meanwhile, species that hypodermically inject sperm lack bristles, potentially as an adaptation to the environment experienced by hypodermic sperm. Combining functional annotations from the model, M. lignano, with transcriptomes from 97 congeners, we find genus-wide faster sequence evolution in reproduction-related versus ubiquitously-expressed genes, consistent with stronger sexual selection on the former. Additionally, species with hypodermic sperm morphologies had elevated molecular sequence evolution, regardless of a genes functional annotation. These genome-wide patterns suggest reduced selection efficiency following shifts to hypodermic mating, possibly due to higher selfing rates in these species. Moreover, we find little evidence for convergent amino acid changes across species. Our work not only shows that reproduction-related genes evolve rapidly also in hermaphroditic animals, but also that well-replicated contrasts of different sexual selection contexts can reveal underappreciated genome-wide effects.

evolutionary biology↗

Frequent origins of traumatic insemination involve convergent shifts in sperm and genital morphology

Traumatic insemination is a mating behaviour 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 canalising effect on morphology. Signatures of male-female coevolution 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.

evolutionary biology↗