Mating ecology explains patterns of genome elimination

This research has been supported by a Royal Society University Research Fellowship (AG), a Royal Society Newton International Fellowship (LR) and two NERC Independent Research Fellowships (AG & LR).Genome elimination – whereby an individual discards chromosomes inherited from one parent, and transmits only those inherited from the other parent – is found across thousands of animal species. It is more common in association with inbreeding, under male heterogamety, in males, and in the form of paternal genome elimination. However, the reasons for this broad pattern remain unclear. We develop a mathematical model to determine how degree of inbreeding, sex determination, genomic location, pattern of gene expression and parental origin of the eliminated genome interact to determine the fate of genome-elimination alleles. We find that: inbreeding promotes paternal genome elimination in the heterogametic sex; this may incur population extinction under female heterogamety, owing to eradication of males; and extinction is averted under male heterogamety, owing to countervailing sex-ratio selection. Thus, we explain the observed pattern of genome elimination. Our results highlight the interaction between mating system, sex-ratio selection and intragenomic conflict.Publisher PDFPeer reviewe

How to make a haploid male

Funding: Natural Environment Research Council Independent Research Fellowship (NE/K009524/1); European Research Council Consolidator Grant (771387) (AG).Haplodiploidy has evolved repeatedly among invertebrates, and appears to be associated with inbreeding. Evolutionary biologists have long debated the possible benefits for females in diplodiploid species to produce haploid sons–beginning their population's transition to haplodiploidy–and whether inbreeding promotes or inhibits this transition. However, little attention has been given to what makes a haploid individual male rather than female, and whether the mechanism of sex determination may modulate the costs and benefits of male haploidy. We remedy this by performing a theoretical analysis of the origin and invasion of male haploidy across the full range of sex‐determination mechanisms and sib‐mating rates. We find that male haploidy is facilitated by three different mechanisms of sex determination–all involving male heterogamety–and impeded by the others. We also find that inbreeding does not pose an obvious evolutionary barrier, on account of a previously neglected sex‐ratio effect whereby the production of haploid sons leads to an abundance of granddaughters that is advantageous in the context of inbreeding. We find empirical support for these predictions in a survey of sex determination and inbreeding across haplodiploids and their sister taxa.Publisher PDFPeer reviewe

The Tree of Sex consortium: A global initiative for studying the evolution of reproduction in eukaryotes

Reproduction is a fundamental aspect of life that affects all levels of biology, from genomes and development to population dynamics and diversification. The first Tree of Sex database synthesised the vast diversity of reproductive strategies and their intriguing distribution throughout eukaryotes. A decade on, we are reviving this initiative and greatly expanding its scope to provide the most comprehensive integration of knowledge on eukaryotic reproduction to date. In this perspective, we first identify important gaps in our current knowledge of reproductive strategies across eukaryotes. We then highlight a selection of questions that will benefit most from this new Tree of Sex project, including those related to the evolution of sex, modes of sex determination, sex chromosomes, and the consequences of various reproductive strategies. Finally, we outline our vision for the new Tree of Sex database and the consortium that will create it (treeofsex.ac.uk). The new database will cover all Eukaryota and include a wide selection of biological traits. It will also incorporate genomic data types that were scarce or non-existent at the time of the first Tree of Sex initiative. The new database will be publicly accessible, stable, and self-sustaining, thus greatly improving the accessibility of reproductive knowledge to researchers across disciplines for years to come. Lastly, the consortium will persist after the database is created to serve as a collaborative framework for research, prioritising ethical standards in the collection, use, and sharing of reproductive data. The new Tree of Sex consortium is open, and we encourage all who are interested in this topic to join us

Does a plant-eating insect's diet govern the evolution of insecticide resistance? Comparative tests of the pre-adaptation hypothesis

According to the pre-adaptation hypothesis, the evolution of insecticide resistance in plant-eating insects co-opts adaptations that initially evolved during chemical warfare with their host plants. Here, we used comparative statistics to test two predictions of this hypothesis: (i) Insects with more diverse diets should evolve resistance to more diverse insecticides. (ii) Feeding on host plants with strong or diverse qualitative chemical defenses should prime an insect lineage to evolve insecticide resistance. Both predictions are supported by our tests. What makes this especially noteworthy is that differences in the diets of plant-eating insect species are typically ignored by the population genetic models we use to make predictions about insecticide resistance evolution. Those models surely capture some of the differences between host-use generalists and specialists, for example, differences in population size and migration rates into treated fields, but they miss other potentially important differences, for example, differences in metabolic diversity and gene expression plasticity. Ignoring these differences could be costly

The evolutionary dynamics of haplodiploidy: genome architecture and haploid viability

Haplodiploid reproduction, in which males are haploid and females are diploid, is widespread among animals, yet we understand little about the forces responsible for its evolution. The current theory is that haplodiploidy has evolved through genetic conflicts, as it provides a transmission advantage to mothers. Male viability is thought to be a major limiting factor; diploid individuals tend to harbor many recessive lethal mutations. This theory predicts that the evolution of haplodiploidy is more likely in male heterogametic lineages with few chromosomes, as genes on the X chromosome are often expressed in a haploid environment, and the fewer the chromosome number, the greater the proportion of the total genome that is X‐linked. We test this prediction with comparative phylogenetic analyses of mites, among which haplodiploidy has evolved repeatedly. We recover a negative correlation between chromosome number and haplodiploidy, find evidence that low chromosome number evolved prior to haplodiploidy, and that it is unlikely that diplodiploidy has reevolved from haplodiploid lineages of mites. These results are consistent with the predicted importance of haploid male viability