Paternal genome elimination (PGE) is a non-Mendelian inheritance system, described in numerous arthropod species, in which males develop from fertilized eggs, but their paternally inherited chromosomes are eliminated before or during spermatogenesis. Therefore, PGE males only transmit their maternally inherited set of chromosomes to their offspring. In addition to the elimination of paternal chromosomes, diverse PGE species have also repeatedly evolved the transcriptional silencing of the paternal genome, making males effectively haploid. However, it is unclear if this paternal chromosome silencing is mechanistically linked to the chromosome elimination or has evolved at a later stage, and if so, what drives the haploidization of males under PGE. In order to understand these questions, here we study the human louse, Pediculus humanus, which represents an ideal model system, as it appears to be the only instance of PGE where males eliminate, but not silence their paternal chromosomes, although the latter remains to be shown conclusively. In this study, we analyzed parent-of-origin allele-specific expression patterns in male offspring of crosses between head and body lice ecotypes. We show that hybrid adult males of P. humanus display biparental gene expression, which constitutes the first case of a species with PGE in which genetic activity of paternal chromosomes in the soma is not affected by embryonic silencing or (partial or complete) elimination. We did however also identify a small number of maternally biased genes (potentially imprinted genes), which may be involved in the elimination of paternal chromosomes during spermatogenesis. Finally, we have identified genes that show ecotype-specific expression bias. Given the low genetic diversity between ecotypes, this is suggestive for a role of epigenetic processes in ecotype differences.

How repeatable is evolution at genomic and phenotypic scales? We studied the repeatability of evolution during 8 generations of colonization using replicated microcosm experiments with the red flour beetle, Tribolium castaneum. Based on the patterns of shared allele frequency changes that occurred in populations from the same generation or experimental location, we found adaptive evolution to be more repeatable in the introduction and establishment phases of colonization than in the spread phase, when populations expand their range. Lastly, by studying changes in allele frequencies at conserved loci, we found evidence for the theoretical prediction that range expansion reduces the efficiency of selection to purge deleterious alleles. Overall, our results increase our understanding of adaptive evolution during colonization, demonstrating that evolution can be highly repeatable while also showing that stochasticity still plays an important role.

Genetic variation for disease resistance within host populations can strongly impact the spread of endemic pathogens. In plants, recent work has shown that within-population variation in resistance can also affect the transmission of foreign spillover pathogens if that resistance is general. However, most hosts also possess specific resistance mechanisms that provide strong defenses against coevolved endemic pathogens. Here we use a modeling approach to ask how antagonistic coevolution between hosts and their endemic pathogen at the specific resistance locus can affect the frequency of general resistance, and therefore a host's vulnerability to foreign pathogens. We develop a two-locus model with variable recombination that incorporates both general resistance (effective against all pathogens) and specific resistance (effective against endemic pathogens only). With coevolution, when pathogens can evolve to evade specific resistance, we find that the regions where general resistance can evolve are greatly expanded, decreasing the risk of foreign pathogen invasion. Furthermore, coevolution greatly expands the conditions that maintain polymorphisms at both resistance loci, thereby driving greater genetic diversity within host populations. This genetic diversity often leads to positive correlations between host resistance to foreign and endemic pathogens, similar to those observed in natural populations. However, if resistance loci become linked, the resistance correlations can shift to negative. If we include a third linkage-modifying locus in our model, we find that selection often favors complete linkage. Our model demonstrates how coevolutionary dynamics with an endemic pathogen can mold the resistance structure of host populations in ways that affect its susceptibility to foreign pathogen spillovers, and that the nature of these outcomes depends on resistance costs, as well as the degree of linkage between resistance genes.

Whether and how the spatial arrangement of a population influences adaptive evolution has puzzled evolutionary biologists. Theoretical models make conflicting predictions about the probability that a beneficial mutation will become fixed in a population for certain topologies like stars, in which "leaf" populations are connected through a central "hub." To date, these predictions have not been evaluated under realistic experimental conditions. Here, we test the prediction that topology can change the dynamics of fixation both in vitro and in silico by tracking the frequency of a beneficial mutant under positive selection as it spreads through networks of different topologies. Our results provide empirical support that meta-population topology can increase the likelihood that a beneficial mutation spreads, broaden the conditions under which this phenomenon is thought to occur, and points the way toward using network topology to amplify the effects of weakly favored mutations under directed evolution in industrial applications.

Understanding the capacity of pathogens to cause severe disease is of fundamental importance to human health and the preservation of biodiversity. Many of those pathogens are not only transmitted horizontally between unrelated hosts but also vertically between parents and their progeny. It is widely accepted that vertical transmission leads to the evolution of less virulent pathogens, but this idea stems from research that neglects the evolutionary response of hosts. Here, we use a game-theory model of coevolution between pathogen and host to show that vertical transmission does not always lead to more benign pathogens. We highlight scenarios in which vertical transmission results in pathogens exhibiting more virulence. However, we also predict that more benign outcomes are still possible (a) when generating new horizontal infections inflicts too much damage on hosts, (b) when clearing an infection is too costly for the host, and (c) when vertical transmission is promoted by a greater growth rate of the host population. Though our work offers a new perspective on the role of vertical transmission in pathogen-host systems, it does agree with previous experimental work.

Laboratory experiments have suggested that bacteria perform a range of cooperative behaviors, which are favored because they are directed toward relatives (kin selection). However, there is a lack of evidence for cooperation and kin selection in natural bacterial populations. Molecular population genetics offers a promising method to study natural populations because the theory predicts that kin selection will lead to relaxed selection, which will result in increased polymorphism and divergence at cooperative genes. Examining a natural population of Bacillus subtilis, we found consistent evidence that putatively cooperative traits have higher polymorphism and greater divergence than putatively private traits expressed at the same rate. In addition, we were able to eliminate alternative explanations for these patterns and found more deleterious mutations in genes controlling putatively cooperative traits. Overall, our results suggest that cooperation is favored by kin selection, with an average relatedness of r = .79 between interacting individuals.

Mutation is the ultimate source of all genetic variation, and over the last 10 years the ready availability of whole-genome sequencing has permitted direct estimation of mutation rate for many non-model species across the tree of life. In this meta-analysis, we make a comprehensive search of the literature for mutation rate estimates in eukaryotes, identifying 140 mutation accumulation (MA) and parent-offspring (PO) sequencing studies covering 134 species. Based on these data, we revisit differences in the single-nucleotide mutation (SNM) rate between different phylogenetic lineages and update the known relationships between mutation rate and generation time, genome size, and nucleotide diversity-while accounting for phylogenetic nonindependence. We do not find a significant difference between MA and PO in estimated mutation rates, but we confirm that mammal and plant lineages have higher mutation rates than arthropods and that unicellular eukaryotes have the lowest mutation rates. We find that mutation rates are higher in species with longer generation times and larger genome sizes, even when accounting for phylogenetic relationships. Moreover, although nucleotide diversity is positively correlated with mutation rate, the gradient of the relationship is significantly less than one (on a logarithmic scale), consistent with higher mutation rates in populations with smaller effective size. For the 29 species for which data are available, we find that indel mutation rates are positively correlated with nucleotide mutation rates and that short deletions are generally more common than short insertions. Nevertheless, despite recent progress, no estimates of either SNM or indel mutation rates are available for the majority of deeply branching eukaryotic lineages-or even for most animal phyla. Even among charismatic megafauna, experimental mutation rate estimates remain unknown for amphibia and scarce for reptiles and fish.

Coprophagy is a behavior where animals consume feces, and has been observed across a wide range of species, including birds and mammals. The phenomenon is particularly prevalent in juveniles, but the reasons for this remain unclear. One hypothesis is that coprophagy enables offspring to acquire beneficial gut microbes that aid development. However, despite the potential importance of this behavior, studies investigating the effects in juveniles are rare. Here we experimentally test this idea by examining how ingestion of adult feces by ostrich chicks affects their gut microbiota development, growth, feeding behavior, pathogen abundance, and mortality. We conducted extensive longitudinal experiments for 8 weeks, repeated over 2 years. It involved 240 chicks, of which 128 were provided daily access to fresh fecal material from adults and 112 were simultaneously given a control treatment. Repeated measures, behavioral observations, and DNA metabarcoding of the microbial gut community, both prior to and over the course of the experiment, allowed us to evaluate multiple aspects of the behavior. The results show that coprophagy causes (a) marked shifts to the juvenile gut microbiota, including a major increase in diversity and rapid maturation of the microbial composition, (b) higher growth rates (fecal-supplemented chicks became 9.4% heavier at 8 weeks old), (c) changes to overall feeding behavior but no differences in feed intake, (d) lower abundance of a common gut pathogen (Clostridium colinum), and (e) lower mortality associated with gut disease. Together, our results suggest that the behavior of coprophagy in juveniles is highly beneficial and may have evolved to accelerate the development of gut microbiota.

One of the most pressing questions we face as biologists is to understand how climate change will affect the evolutionary dynamics of natural populations and how these dynamics will in turn affect population recovery. Increasing evidence shows that sexual selection favors population viability and local adaptation. However, sexual selection can also foster sexual conflict and drive the evolution of male harm to females. Male harm is extraordinarily widespread and has the potential to suppress female fitness and compromise population growth, yet we currently ignore its net effects across taxa or its influence on local adaptation and evolutionary rescue. We conducted a comparative meta-analysis to quantify the impact of male harm on female fitness and found an overall negative effect of male harm on female fitness. Negative effects seem to depend on proxies of sexual selection, increasing inversely to the female relative size and in species with strong sperm competition. We then developed theoretical models to explore how male harm affects adaptation and evolutionary rescue. We show that, when sexual conflict depends on local adaptation, population decline is reduced, but at the cost of slowing down genetic adaptation. This trade-off suggests that eco-evolutionary feedback on sexual conflict can act like a double-edged sword, reducing extinction risk by buffering the demographic costs of climate change, but delaying genetic adaptation. However, variation in the mating system and male harm type can mitigate this trade-off. Our work shows that male harm has widespread negative effects on female fitness and productivity, identifies potential mechanistic factors underlying variability in such costs across taxa, and underscores how acknowledging the condition-dependence of male harm may be important to understand the demographic and evolutionary processes that impact how species adapt to environmental change.

Tropical islands are renowned as natural laboratories for evolutionary study. Lineage radiations across tropical archipelagos are ideal systems for investigating how colonization, speciation, and extinction processes shape biodiversity patterns. The expansion of the island thrush across the Indo-Pacific represents one of the largest yet most perplexing island radiations of any songbird species. The island thrush exhibits a complex mosaic of pronounced plumage variation across its range and is arguably the world’s most polytypic bird. It is a sedentary species largely restricted to mountain forests, yet it has colonized a vast island region spanning a quarter of the globe. We conducted a comprehensive sampling of island thrush populations and obtained genome-wide SNP data, which we used to reconstruct its phylogeny, population structure, gene flow, and demographic history. The island thrush evolved from migratory Palearctic ancestors and radiated explosively across the Indo-Pacific during the Pleistocene, with numerous instances of gene flow between populations. Its bewildering plumage variation masks a biogeographically intuitive stepping stone colonization path from the Philippines through the Greater Sundas, Wallacea, and New Guinea to Polynesia. The island thrush’s success in colonizing Indo-Pacific mountains can be understood in light of its ancestral mobility and adaptation to cool climates; however, shifts in elevational range, degree of plumage variation and apparent dispersal rates in the eastern part of its range raise further intriguing questions about its biology.