The role of conflict in the formation and maintenance of variant sex chromosome systems in mammals.

The XX/XY sex chromosome system is deeply conserved in therian mammals, as is the role of Sry in testis determination, giving the impression of stasis relative to other taxa. However, the long tradition of cytogenetic studies in mammals documents sex chromosome karyotypes that break this norm in myriad ways, ranging from fusions between sex chromosomes and autosomes to Y chromosome loss. Evolutionary conflict, in the form of sexual antagonism or meiotic drive, is the primary predicted driver of sex chromosome transformation and turnover. Yet conflict-based hypotheses are less considered in mammals, perhaps because of the perceived stability of the sex chromosome system. To address this gap, we catalogue and characterize all described sex chromosome variants in mammals, test for family-specific rates of accumulation, and consider the role of conflict between the sexes or within the genome in the evolution of these systems. We identify 152 species with sex chromosomes that differ from the ancestral state and find evidence for different rates of ancestral to derived transitions among families. Sex chromosome-autosome fusions account for 80% of all variants whereas documented sex chromosome fissions are limited to three species. We propose that meiotic drive and drive suppression provide viable explanations for the evolution of many of these variant systems, particularly those involving autosomal fusions. We highlight taxa particularly worthy of further study and provide experimental predictions for testing the role of conflict and its alternatives in generating observed sex chromosome diversity.

The genomic landscape, causes, and consequences of extensive phylogenomic discordance in Old World mice and rats.

A species tree is a central concept in evolutionary biology whereby a single branching phylogeny reflects relationships among species. However, the phylogenies of different genomic regions often differ from the species tree. Although tree discordance is often widespread in phylogenomic studies, we still lack a clear understanding of how variation in phylogenetic patterns is shaped by genome biology or the extent to which discordance may compromise comparative studies. We characterized patterns of phylogenomic discordance across the murine rodents (Old World mice and rats) - a large and ecologically diverse group that gave rise to the mouse and rat model systems. Combining new linked-read genome assemblies for seven murine species with eleven published rodent genomes, we first used ultra-conserved elements (UCEs) to infer a robust species tree. We then used whole genomes to examine finer-scale patterns of discordance and found that phylogenies built from proximate chromosomal regions had similar phylogenies. However, there was no relationship between tree similarity and local recombination rates in house mice, suggesting that genetic linkage influences phylogenetic patterns over deeper timescales. This signal may be independent of contemporary recombination landscapes. We also detected a strong influence of linked selection whereby purifying selection at UCEs led to less discordance, while genes experiencing positive selection showed more discordant and variable phylogenetic signals. Finally, we show that assuming a single species tree can result in high error rates when testing for positive selection under different models. Collectively, our results highlight the complex relationship between phylogenetic inference and genome biology and underscore how failure to account for this complexity can mislead comparative genomic studies.

Tracking Chromosomal Origins in the Northern Italy System of Metacentric Races of the House Mouse.

The Western European house mouse is chromosomally diverse, with diploid karyotypes ranging from the standard 40 telocentric chromosomes down to 22 chromosomes. Karyotypes are modified through Robertsonian (Rb) fusion of 2 telocentrics into a single metacentric, occurring repeatedly with fixation, and whole-arm reciprocal translocations (WARTs) generating additional novel karyotypes. Over 100 metacentric populations (chromosomal races) have been identified, geographically clustered into "systems." Chromosomal races within systems often hybridise, and new races may emerge through this hybridisation ("zonal raciation"). We wished to determine the degree to which chromosomal races in a system have evolved independently or share common ancestry. Recombination between chromosomes from hybridising chromosomal races can erase the signals associated with a particular metacentric of interest, making inferences challenging. However, reduced recombination near the centromeres of chromosomal race-specific metacentrics makes centromere-adjacent markers ideal for solving this problem. For the Northern Italy System (NIS), we used microsatellite markers near the centromere to test previous hypotheses about evolutionary relationships of 5 chromosomal races. We chose markers from chromosomes 1, 3, 4, and 6, all of which comprise one arm of a metacentric in at least 2 of these NIS metacentric populations. We used estimates of FST and RST, as well as principal components analyses and neighbour-joining phylogenetic analyses, to infer evolutionary relationships between these 5 chromosomal races and neighbouring mice with the standard karyotype. We showed that the metacentric populations form a single grouping distinct from the standard populations, consistent with their common origin and consistent with a parsimonious sequence of chromosomal rearrangements to explain the relationship of the chromosomal races. That origin and evolution of the chromosomal races in the system would have involved Rb fusions, explaining the occurrence of chromosomal races with diploid numbers as low as 22. However, WARTs and zonal raciation have also been inferred, and the rare occurrence of chromosome 1 in different metacentrics in closely related chromosomal races is almost certainly explained by a WART. Our results with centromeric microsatellites are consistent with the above scenarios, illustrating, once again, the value of markers in the centromeric region to test evolutionary hypotheses in house mouse chromosomal systems.

Population structure and inbreeding in wild house mice (Mus musculus) at different geographic scales.

House mice (Mus musculus) have spread globally as a result of their commensal relationship with humans. In the form of laboratory strains, both inbred and outbred, they are also among the most widely used model organisms in biomedical research. Although the general outlines of house mouse dispersal and population structure are well known, details have been obscured by either limited sample size or small numbers of markers. Here we examine ancestry, population structure, and inbreeding using SNP microarray genotypes in a cohort of 814 wild mice spanning five continents and all major subspecies of Mus, with a focus on M. m. domesticus. We find that the major axis of genetic variation in M. m. domesticus is a south-to-north gradient within Europe and the Mediterranean. The dominant ancestry component in North America, Australia, New Zealand, and various small offshore islands are of northern European origin. Next we show that inbreeding is surprisingly pervasive and highly variable, even between nearby populations. By inspecting the length distribution of homozygous segments in individual genomes, we find that inbreeding in commensal populations is mostly due to consanguinity. Our results offer new insight into the natural history of an important model organism for medicine and evolutionary biology.

Ecological selectivity and the evolution of mammalian substrate preference across the K-Pg boundary.

The Cretaceous-Paleogene (K-Pg) mass extinction 66 million years ago was characterized by a worldwide ecological catastrophe and rapid species turnover. Large-scale devastation of forested environments resulting from the Chicxulub asteroid impact likely influenced the evolutionary trajectories of multiple clades in terrestrial environments, and it has been hypothesized to have biased survivorship in favour of nonarboreal lineages across the K-Pg boundary. Here, we evaluate patterns of substrate preferences across the K-Pg boundary among crown group mammals, a group that underwent rapid diversification following the mass extinction. Using Bayesian, likelihood, and parsimony reconstructions, we identify patterns of mammalian ecological selectivity that are broadly similar to those previously hypothesized for birds. Models based on extant taxa indicate predominant K-Pg survivorship among semi- or nonarboreal taxa, followed by numerous independent transitions to arboreality in the early Cenozoic. However, contrary to the predominant signal, some or all members of total-clade Euarchonta (Primates + Dermoptera + Scandentia) appear to have maintained arboreal habits across the K-Pg boundary, suggesting ecological flexibility during an interval of global habitat instability. We further observe a pronounced shift in character state transitions away from plesiomorphic arboreality associated with the K-Pg transition. Our findings are consistent with the hypothesis that predominantly nonarboreal taxa preferentially survived the end-Cretaceous mass extinction, and emphasize the pivotal influence of the K-Pg transition in shaping the early evolutionary trajectories of extant terrestrial vertebrates.