Daniel L. Jeffries’s research while affiliated with University of Bern and other places

The genetic basis of sex determination is typically conserved within species if not within broader lineages. For example, within the stickleback family (Gasterosteidae), AmhY has been identified as a master sex‐determination (MSD) gene in multiple species across two genera. By contrast, the existence of within‐species variability in the genetic basis of sex determination is not frequently observed but provides an opportunity to understand the evolution and turnover of sex determination systems. In this study, we investigated the consistency with which AmhY is involved in sex determination across 610 individuals from five brook stickleback (Culaea inconstans) populations. We designed a PCR‐restriction enzyme assay to identify the presence of AmhY in each individual and recorded sexual morphology in each individual in the field at the time of capture. We found that the genetic sex (presence/absence of AmhY) did not match the field‐determined phenotypic sex in up to 44% of individuals within a population. This variation in the genetic basis of sex determination in brook stickleback suggests that the mechanism of sex determination in this species is likely more complex than thought when AmhY was first implicated and may still be evolving. Such within‐species variation provides an opportunity to further investigate how and why transitions in sex‐determination mechanisms occur.

Hybridization plays a pivotal role in evolution, influencing local adaptation and speciation. However, it can also reduce biodiversity, which is especially damaging when native and non‐native species meet. Hybridization can threaten native species via competition (with vigorous hybrids), reproductive resource wastage and gene introgression. The latter, in particular, could result in increased fitness in invasive species, decreased fitness of natives and compromise reintroduction or recovery conservation practices. In this study, we use a combination of RAD sequencing and microsatellites for a range‐wide sample set of 1366 fish to evaluate the potential for hybridization and introgression between native crucian carp ( Carassius carassius ) and three non‐native taxa ( Carassius auratus auratus , Carassius auratus gibelio and Cyprinus carpio ) in European water bodies. We found hybridization between native and non‐native taxa in 82% of populations with non‐natives present, highlighting the potential for substantial ecological impacts from hybrids on crucian carp populations. However, despite such high rates of hybridization, we could find no evidence of introgression between these taxa. The presence of triploid backcrosses in at least two populations suggests that the lack of introgression among these taxa is likely due to meiotic dysfunction in hybrids, leading to the production of polyploid offspring which are unable to reproduce sexually. This result is promising for crucian reintroduction programs, as it implies limited risk to the genetic integrity of source populations. Future research should investigate the reproductive potential of triploid hybrids and the ecological pressures hybrids impose on C. carassius .

Sexual reproduction, while often associated with separate sexes, is an ancient and widespread feature of multicellular eukaryotes. While a diversity of sex determination mechanisms exist, for many organisms, which of these mechanisms is used remains unknown. Exploring sex determination mechanisms in Acariformes, among the oldest chelicerate clades, is intriguing due to its potential to unveil conserved sex determination systems. This insight can have implications for understanding sex chromosome evolution and its broader impact on higher taxa.To identify the mechanism of sex determination in Acari, i.e., oribatid mites, we generated a high-quality chromosome-level genome assembly of Hermannia gibba (Koch, 1839) by combining PacBio HiFi and Hi-C sequencing. Coverage and allele-frequency analyses on pools of male and female individuals suggest a female-heterogametic ZW sex-determination system with little degeneration of the W chromosome. To date, this represents the only documented case of a ZW system in Acariformes. Further comparative studies in H. gibba will reveal how old the ZW system is and whether it exhibits conservation or polymorphism.

Sex chromosomes vary greatly in their age and levels of differentiation across the tree of life. This variation is largely due to the rates of sex chromosome turnover in different lineages; however, we still lack an explanation for why sex chromosomes are so conserved in some lineages (e.g. mammals, birds) but so labile in others (e.g. teleosts, amphibians). To identify general mechanisms driving transitions in sex determination systems or forces which favour their conservation, we first require empirical data on sex chromosome systems from multiple lineages. Stickleback fishes are a valuable model lineage for the study of sex chromosome evolution due to variation in sex chromosome systems between closely-related species. Here, we identify the sex chromosome and a strong candidate for the master sex determination gene in the brook stickleback, Culaea inconstans. Using whole-genome sequencing of wild-caught samples and a lab cross, we identify AmhY, a male specific duplication of the gene Amh, as the candidate master sex determination gene. AmhY resides on Chromosome 20 in C. inconstans and is likely a recent duplication, as both AmhY and the sex-linked region of Chromosome 20 show little sequence divergence. Importantly, this duplicate AmhY represents the second independent duplication and recruitment of Amh as the sex determination gene in stickleback and the eighth example known across teleosts. We discuss this convergence in the context of sex chromosome turnovers and the role that the Amh/AmhrII pathway, which is crucial for sex determination, may play in the evolution of sex chromosomes in teleosts.

Sex chromosomes constantly exist in a dynamic state of evolution: rapid turnover and change of heterogametic sex during homomorphic state, and often stepping out to a heteromorphic state followed by chromosomal decaying. However, the forces driving these different trajectories of sex chromosome evolution are still unclear. The Japanese frog Glandirana rugosa is one taxon well suited to the study on these driving forces. The species has two different heteromorphic sex chromosome systems, XX‐XY and ZZ‐ZW, which are separated in different geographic populations. Both XX‐XY and ZZ‐ZW sex chromosomes are represented by chromosome 7 (2n = 26). Phylogenetically, these two systems arose via hybridization between two ancestral lineages of West Japan and East Japan populations, of which sex chromosomes are homomorphic in both sexes and to date have not yet been identified. Identification of the sex chromosomes will give us important insight into the mechanisms of sex chromosome evolution in this species. Here, we used a high‐throughput genomic approach to identify the homomorphic XX‐XY sex chromosomes in both ancestral populations. Sex‐linked DNA markers of West Japan were aligned to chromosome 1, whereas those of East Japan were aligned to chromosome 3. These results reveal that at least two turnovers across three different sex chromosomes 1, 3 and 7 occurred during evolution of this species. This finding raises the possibility that cohabitation of the two different sex chromosomes from ancestral lineages induced turnover to another new one in their hybrids, involving transition of heterogametic sex and evolution from homomorphy to heteromorphy.

Sex chromosomes vary greatly in their age and levels of differentiation across the tree of life. This variation is largely due to the rates of sex chromosome turnover in different lineages; however, we still lack an explanation for why sex chromosomes are so conserved in some lineages (e.g. Mammals, Birds) but so labile in others (e.g. Fish, Amphibians). Here we add to the information on sex chromosomes in stickleback, a valuable model lineage for the study of sex chromosome evolution, by identifying the sex chromosome and a strong candidate for the master sex determination gene in the brook stickleback, Culaea inconstans . Using whole genome sequencing of wild-caught samples and a lab cross, we identify AmhY , a male specific duplication of the gene Amh, as the candidate master sex determination gene. AmhY resides on Chromosome 20 in C. inconstans and is likely a recent duplication, as both AmhY and the sex linked region of Chromosome 20 show little sequence divergence. Importantly, this duplicate AmhY represents the second independent duplication and recruitment of Amh as the sex determination gene in stickleback and the eighth example now known across teleosts. We discuss this convergence in the context of sex chromosome turnovers and the role that the Amh/AmhrII pathway, which is crucial for sex determination, may play in the evolution of sex chromosomes in teleosts.

Reproductive isolation is instrumental to the formation of new species (speciation), but it remains largely enigmatic how many incompatibilities are required to prevent hybridization and where they lie across the genome. By studying patterns of admixture in amphibian hybrid zones, we found that reproductive isolation is initiated by numerous small-effect incompatibilities scattered across the genome rather than concentrated in a few important genes. Unlike mammals and birds, in which Y/W degeneracy is a major cause of hybrid dysfunctions, the undifferentiated sex chromosomes of amphibians do not always host more genetic incompatibilities than other chromosomes. These combined results might explain why amphibian speciation is relatively slow, and its clock-like dynamics offer practical perspectives to categorize evolutionary lineages into species or subspecies.

Until recently, the field of sex chromosome evolution has been dominated by the canonical unidirectional scenario, first developed by Muller in 1918. This model postulates that sex chromosomes emerge from autosomes by acquiring a sex-determining locus. Recombination reduction then expands outwards from this locus, to maintain its linkage with sexually antagonistic/advantageous alleles, resulting in Y or W degeneration and potentially culminating in their disappearance. Based mostly on empirical vertebrate research, we challenge and expand each conceptual step of this canonical model and present observations by numerous experts in two parts of a theme issue of Phil. Trans. R. Soc. B. We suggest that greater theoretical and empirical insights into the events at the origins of sex-determining genes (rewiring of the gonadal differentiation networks), and a better understanding of the evolutionary forces responsible for recombination suppression are required. Among others, crucial questions are: Why do sex chromosome differentiation rates and the evolution of gene dose regulatory mechanisms between male versus female heterogametic systems not follow earlier theory? Why do several lineages not have sex chromosomes? And: What are the consequences of the presence of (differentiated) sex chromosomes for individual fitness, evolvability, hybridization and diversification? We conclude that the classical scenario appears too reductionistic. Instead of being unidirectional, we show that sex chromosome evolution is more complex than previously anticipated and principally forms networks, interconnected to potentially endless outcomes with restarts, deletions and additions of new genomic material. This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)’.