Daven C. Presgraves

Meiotic drivers are selfish genetic elements that gain transmission advantages by distorting equal, Mendelian segregation. For decades, biologists have considered meiotic drivers as interesting, albeit esoteric, case studies. It is now clear, however, that meiotic drive is more common and phylogenetically widespread than previously supposed. Indeed, intensive study of a few well-known cases has begun to reveal the evolutionary genomic consequences of meiotic drive. We argue here that many features of genome evolution, content, and organization that are seemingly inexplicable by organismal adaptation or nearly neutral processes are instead best accounted for by recurrent histories of meiotic drive. We review how meiotic drive can affect the evolution of sequences, gene copy numbers, genes with functions in meiosis and gametogenesis, signatures of “selection,” chromosome rearrangements, and karyotype evolution. We also explore the interactions of meiotic drive elements with other classes of selfish genetic elements, including satellite DNAs, transposable elements, and with the endogenous host genes involved in drive suppression. Finally, we argue that some aspects of drive-mediated genome evolution are now sufficiently well established that we might reverse the direction of discovery—rather than ask how drive affects genome evolution, we can use genome data to discover new putative drive elements.

The standard model of sex chromosome evolution is based on ancient XY or ZW systems. Young neo-sex chromosomes that form via the translocation of autosomal material to preexisting sex chromosomes provide materials to study early events in sex chromosome evolution. Neo-sex chromosomes are taxonomically widespread but, until recently, appeared to be rare in female-heterogametic taxa, including birds. Here, we report on the comparative evolutionary genomics of newly discovered neo-Z and neo-W sex chromosomes in two Pacific Island birds, the honeyeater species, Myzomela tristrami and M. cardinalis . Our results show that 19 to 21 Mya, ~85% of chr5 , an autosome, translocated to the pseudoautosomal region (PAR) of an ancestral sex chromosome (Z or W) and rapidly recombined onto its heterolog, leaving the remainder of chr5 to segregate as a remnant autosome. A large inversion then established a nonrecombining (NR) neo-W region and a neo-PAR. The accumulation of at least seven additional inversions created interspersed blocks of ancestral and neo-W sequence, without expanding the NR region. The neo-W experienced mass invasion by endogenous retrovirus repeats, a reduced efficacy of selection, and functional degeneration. Many of our observations are consistent with predictions of the standard model, whereas others highlight idiosyncrasies of neo-sex chromosomes that arise via translocation of autosomal sequence to ancestral sex chromosomes. We speculate, in particular, that the repository of retrotransposons on the ancestral W may have been an accelerant in the evolution of neo-W structure, content, and functional degeneration.

Secondary contact between closely related taxa represents a “moment of truth” for speciation—an opportunity to test the efficacy of reproductive isolation that evolved in allopatry and to identify the genetic, behavioral, and/or ecological barriers that separate species in sympatry. Sex chromosomes are known to rapidly accumulate differences between species, an effect that may be exacerbated for neo-sex chromosomes that are transitioning from autosomal to sex-specific inheritance. Here we report that, in the Solomon Islands, two closely related bird species in the honeyeater family—Myzomela cardinalis and Myzomela tristrami—carry neo-sex chromosomes and have come into recent secondary contact after ~1.1 my of geographic isolation. Hybrids of the two species were first observed in sympatry ~100 years ago. To determine the genetic consequences of hybridization, we use population genomic analyses of individuals sampled in allopatry and in sympatry to characterize gene flow in the contact zone. Using genome-wide estimates of diversity, differentiation, and divergence, we find that the degree and direction of introgression varies dramatically across the genome. For sympatric birds, autosomal introgression is bidirectional, with phenotypic hybrids and phenotypic parentals of both species showing admixed ancestry. In other regions of the genome, however, the story is different. While introgression on the Z/neo-Z-linked sequence is limited, introgression of W/neo-W regions and mitochondrial sequence (mtDNA) is highly asymmetric, moving only from the invading M. cardinalis to the resident M. tristrami. The recent hybridization between these species has thus enabled gene flow in some genomic regions but the interaction of admixture, asymmetric mate choice, and/or natural selection has led to the variation in the amount and direction of gene flow at sex-linked regions of the genome.

Secondary contact between closely related taxa represents a “moment of truth” for speciation. Removal of geographic barriers allows us to test the strength of reproductive isolation that evolved in allopatry and identify the genetic, behavioral, and/or ecological barriers that separate species in sympatry. Sex chromosomes are known to rapidly accumulate differences between species, an effect that may be exacerbated for neo-sex chromosomes because they are regions of the genome that have recently become linked to sex chromosomes and are transitioning from autosomal to sex-specific inheritance. Two closely related bird species in the honeyeater family — Myzomela cardinalis and Myzomela tristrami — carry neo-sex chromosomes and have come into recent secondary contact in the Solomon Islands after being isolated for ∼3 my. Hybrids of these two species have been observed in sympatry for at least 100 years. To determine the genetic consequences of hybridization, we use population genomic analyses of individuals sampled in allopatry and sympatry to characterize gene flow in the contact zone. Using genome-wide estimates of diversity, differentiation, and divergence, we find that the degree and direction of introgression varies dramatically across the genome. Autosomal introgression is bidirectional, with phenotypic hybrids and phenotypic parentals of both species showing admixed ancestry. On the sex and neo-sex chromosomes, the story is different. Introgression of Z is limited and neo-Z sequence shows no evidence of introgression, whereas introgression of W and neo-W is strong but highly asymmetric, moving only from the invasive M. cardinalis to the resident M. tristrami . Thus, reproductive isolation is incomplete, but sex and neo-sex chromosome regions have prevented gene flow in one (W/neo-W) or both (Z/neo-Z) directions. The recent contact between previously isolated species indicates that hybridization may permit gene flow between taxa in some genomic regions, but species divergence can be maintained by barriers to gene flow associated with rapidly evolving sex-linked regions of the genome. Author Summary: When a new species colonizes an island and interacts with a closely related native species, we are provided with a rare opportunity to identify the factors that keep species distinct and the consequences of interbreeding. Regions of the genome that evolve rapidly or influence mate choice may be especially likely to act as barriers to gene flow. The red Myzomela cardinalis, birds in the honeyeater family, have recently arrived to Makira in the Solomon Islands, joining the endemic, all black Myzomela tristrami. We used population genomic analyses of individuals in geographic isolation, as well as those in geographic contact with the other species, to understand the history of these two species and the consequences of their recent range overlap on Makira. We found that regions of the genome that are sex-specific ( i.e., sex chromosomes) were either limited in their ability to move between species, or only moved in one direction, from the invading M. cardinalis to the native M. tristrami . This work highlights how certain regions of the genome may be especially important in defining species boundaries and the generation and maintenance of biodiversity.

Meiotic drive supergenes are complexes of alleles at linked loci that together subvert Mendelian segregation resulting in preferential transmission. In males, the most common mechanism of drive involves the disruption of sperm bearing one of a pair of alternative alleles. While at least two loci are important for male drive—the driver and the target—linked modifiers can enhance drive, creating selection pressure to suppress recombination. In this work, we investigate the evolution and genomic consequences of an autosomal, multilocus, male meiotic drive system, Segregation Distorter (SD) in the fruit fly, Drosophila melanogaster. In African populations, the predominant SD chromosome variant, SD-Mal, is characterized by two overlapping, paracentric inversions on chromosome arm 2R and nearly perfect (~100%) transmission. We study the SD-Mal system in detail, exploring its components, chromosomal structure, and evolutionary history. Our findings reveal a recent chromosome-scale selective sweep mediated by strong epistatic selection for haplotypes carrying Sd, the main driving allele, and one or more factors within the double inversion. While most SD-Mal chromosomes are homozygous lethal, SD-Mal haplotypes can recombine with other, complementing haplotypes via crossing over, and with wildtype chromosomes via gene conversion. SD-Mal chromosomes have nevertheless accumulated lethal mutations, excess non-synonymous mutations, and excess transposable element insertions. Therefore, SD-Mal haplotypes evolve as a small, semi-isolated subpopulation with a history of strong selection. These results may explain the evolutionary turnover of SD haplotypes in different populations around the world and have implications for supergene evolution broadly.

Sex chromosomes are susceptible to the evolution of selfish meiotic drive elements that bias transmission and distort progeny sex ratios. Conflict between such sex-ratio drivers and the rest of the genome can trigger evolutionary arms races resulting in genetically suppressed ‘cryptic’ drive systems. The Winters cryptic sex-ratio drive system of Drosophila simulans comprises a driver, Distorter on the X (Dox) and an autosomal suppressor, Not much yang, a retroduplicate of Dox that suppresses via production of endogenous small interfering RNAs (esiRNAs). Here we report that over 22 Dox-like (Dxl) sequences originated, amplified and diversified over the ~250,000-year history of the three closely related species, D. simulans, D. mauritiana and D. sechellia. The Dxl sequences encode a rapidly evolving family of protamines. Dxl copy numbers amplified by ectopic exchange among euchromatic islands of satellite DNAs on the X chromosome and separately spawned four esiRNA-producing suppressors on the autosomes. Our results reveal the genomic consequences of evolutionary arms races and highlight complex interactions among different classes of selfish DNAs.

The three fruitfly species of theDrosophila simulansclade—D. simulans, D. mauritiana, andD. sechellia— have served as important models in speciation genetics for over 40 years. These species are reproductively isolated by geography, ecology, sexual signals, postmating-prezygotic interactions, and postzygotic genetic incompatibilities. All pairwise crosses between these species conform to Haldane’s rule, producing fertile F₁hybrid females and sterile F₁hybrid males. The close phylogenetic proximity of theD. simulansclade species to the model organism,D. melanogaster, has empowered genetic analyses of their species differences, including reproductive incompatibilities. But perhaps no phenotype has been subject to more continuous and intensive genetic scrutiny than hybrid male sterility. Here we review the history, progress, and current state of our understanding of hybrid male sterility among theD. simulansclade species. Our aim is to integrate the available information from experimental and population genetics analyses bearing on the causes and consequences of hybrid male sterility. We highlight numerous conclusions that have emerged as well as issues that remain unresolved. We focus on the special role of sex chromosomes, the fine-scale genetic architecture of hybrid male sterility, and the history of gene flow between species. The biggest surprises to emerge from this work are that (i) genetic conflicts may be an important general force in the evolution of hybrid incompatibility, (ii) hybrid male sterility is polygenic with contributions of complex epistasis, and (iii) speciation, even among these geographically allopatric taxa, has involved the interplay of gene flow, negative selection, and positive selection. These three conclusions are marked departures from the classical views of speciation that emerged from the modern evolutionary synthesis.

Meiotic crossing over ensures proper segregation of homologous chromosomes and generates genotypic diversity. Despite these functions, little is known about the genetic factors and population genetic forces involved in the evolution of recombination rate differences among species. The dicistronic meiosis gene, mei-217/mei-218, mediates most of the species differences in crossover rate and patterning during female meiosis between the closely related fruitfly species, Drosophila melanogaster and D. mauritiana. The MEI-218 protein is one of several meiosis-specific mini-chromosome maintenance (mei-MCM) proteins that form a multi-protein complex essential to crossover formation, whereas the BLM helicase acts as an anti-crossover protein. Here we study the molecular evolution of five genes— mei-218, the other three known members of the mei-MCM complex, and Blm— over the phylogenies of three Drosophila species groups— melanogaster, obscura, and virilis. We then use transgenic assays in D. melanogaster to test if molecular evolution at mei-218 has functional consequences for crossing over using alleles from the distantly related species D. pseudoobscura and D. virilis. Our molecular evolutionary analyses reveal recurrent positive selection at two mei-MCM genes. Our transgenic assays show that sequence divergence among mei-218 alleles from D. melanogaster, D. pseudoobscura, and D. virilis has functional consequences for crossing over. In a D. melanogaster genetic background, the D. pseudoobscura mei-218 allele nearly rescues wildtype crossover rates but alters crossover patterning, whereas the D. virilis mei-218 allele conversely rescues wildtype crossover patterning but not crossover rates. These experiments demonstrate functional divergence at mei-218 and suggest that crossover rate and patterning are separable functions.

During speciation, sex chromosomes often accumulate interspecific genetic incompatibilities faster than the rest of the genome. The drive theory posits that sex chromosomes are susceptible to recurrent bouts of meiotic drive and suppression, causing the evolutionary build-up of divergent cryptic sex-linked drive systems and, incidentally, genetic incompatibilities. To assess the role of drive during speciation, we combine high-resolution genetic mapping of X-linked hybrid male sterility with population genomics analyses of divergence and recent gene flow between the fruitfly species, Drosophila mauritiana and D. simulans. Our findings reveal a high density of genetic incompatibilities and a corresponding dearth of gene flow on the X chromosome. Surprisingly, we find that a known drive element recently migrated between species and, rather than contributing to interspecific divergence, caused a strong reduction in local sequence divergence, undermining the evolution of hybrid sterility. Gene flow can therefore mediate the effects of selfish genetic elements during speciation.