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Hollis, B.

Publications and source records attributed to Hollis, B..

9 recordsLinked to original sources

Natural limits on male mating sustain costly female choice, exaggerated displays, and genetic variation

The persistence of costly female preferences, exaggerated male sexual displays, and the genetic variation underlying those displays remains a central puzzle in evolutionary biology. Classical Fisherian models explain preference-driven display exaggeration but not how costly preference and display can persist without runaway or collapse. These models assume that preferred males remain available regardless of previous mating success, precluding feedback through declining availability. Here I use a gene-centered analysis to show that allelic realized relatedness governs the indirect benefits of choice and that unlimited availability allows relatedness to remain high until genetic variation is lost. Individual-based simulations relaxing this idealization exposed negative feedback: as preference spread and concentrated mating success, preferred males reached capacity and became unavailable. Choosy females became less able to steer indirect fitness benefits toward additional copies of the preference allele, reducing allelic realized relatedness and constraining further evolution of preference and display. This transformed Fisherian runaway into stable exaggeration, allowing costly preference and display to persist for tens of thousands of generations across broad ranges of preference strength, mating capacity, and recombination rate. With autosomal display and a 1% viability cost of preference, stable exaggeration reached 16.5 additive-genetic standard deviations above matched no-preference baselines. Negative feedback generated disruptive selection on display, amplifying additive genetic variation beyond mutation-selection balance by as much as 32-fold, providing a resolution to the lek paradox--the persistence of display variation despite strong sexual selection--without invoking biased mutation or condition dependence. Z linkage of display loci, relevant to birds and other taxa with ZW sex determination, expanded the conditions supporting persistent preference and display, increased exaggeration, and further amplified genetic variation. Once inherent biological limits on male mating success are recognized, Fisherian sexual selection is revealed as a self-regulating form of gene-level cooperation.

evolutionary biology↗

Experimental speciation: selection against hybridization strengthens reproductive barriers and limits introgression

Evolutionary theory predicts that when hybridization between divergent populations is costly, natural selection should favor traits that reduce further interbreeding, a process known as reinforcement. Direct experimental evidence of reinforcement is rare, however, and no study has demonstrated that reinforcing selection can strengthen reproductive isolation between naive populations while allowing continuous gene flow. Here we show that >100 generations of experimental selection against hybridization -- imposed by removing a controlled fraction of GFP-marked hybrids -- led to the evolution of increased reproductive isolation between two naive populations of Drosophila melanogaster. Selection strengthened both sexual isolation (via reduced female remating with migrant males) and postmating-prezygotic isolation, although the specific barriers that evolved depended on the strength of selection against hybridization. Sexual isolation was evident only when females encountered both within-population and migrant males, revealing an important role for social mating context. Notably, intermediate selection against hybridization produced the strongest overall increase in reproductive isolation, suggesting that reinforcement is most effective when maladaptive hybridization with both newly arrived immigrants and early-generation hybrids remains sufficiently common to generate persistent selection for avoidance. Whole-genome sequencing revealed that divergence was concentrated in regions linked to the GFP barrier locus, where introgression was reduced. These regions were also enriched for loci showing signatures consistent with an adaptive response to selection against hybridization. Together, these results provide direct experimental evidence that reinforcement can increase reproductive isolation under ongoing gene flow and reveal how selection against hybridization shapes genomic divergence during the early stages of speciation.

evolutionary biology↗

Vicariance and dispersal shape the colonization history of the Galapagos carpenter bee, Xylocopa darwini

Island colonization and subsequent diversification are often shaped by a complex interplay between organism-specific traits including dispersal capacity and ecological requirements, and the configuration of the landscape over geological time. Here, we investigate the evolutionary history and population genomics of the Galapagos carpenter bee, Xylocopa darwini, across six islands of the Galapagos archipelago. Despite the bees presumed strong flight ability, we find evidence of long-term isolation among all islands with the strongest divergence occurring between the eastern and western islands, and no evidence of contemporary gene flow between any island pairs. Our analyses indicate that the initial colonization of the archipelago by X. darwini occurred during the early Pleistocene, a period when most current islands except for the youngest islands of Isabela and Fernandina, were subaerial, and part of a large contiguous paleo-landmass. Diversification across the Galapagos islands closely tracks the timing of geological separation of the islands, with carpenter bees from the oldest eastern islands splitting first from the western clade over a million years ago. Subsequent diversification of the western clade tracks the sequential fragmentation of the western, central, and southern islands (Isabela, Santiago, Santa Cruz, and Floreana), rather than the geological age of the islands. Despite being on the oldest island, the bee population on Espanola appears to have been founded more recently (within the last 100,000 years) from San Cristobal, providing an exception to diversification tracking paleogeography and is the only example of founding via over-water dispersal among the sampled island populations. Measures of contemporary genetic diversity and runs of homozygosity (ROHs) suggest substantially smaller current population sizes on the southern island of Floreana and the eastern islands of Espanola and San Cristobal. These results are not consistent with a simple relationship between island area and genetic diversity and instead likely reflect a combination of evolution in isolation following vicariance, rare founder events following over-water dispersal, and possible episodes of secondary contact.

evolutionary biology↗

Population-scale sequencing resolves correlates and determinants of latent Epstein-Barr Virus infection

Epstein-Barr Virus (EBV) is an endemic herpesvirus implicated in autoimmunity, cancer, and neurological disorders. Though primary infection typically resolves with subclinical symptoms, long-term complications can arise due to immune dysregulation or viral latency, in which EBV DNA is detectable in blood for decades. Despite the ubiquity of this virus, we have an incomplete understanding of the highly variable responses to EBV that range from asymptomatic infection to a trigger for severe disease. Here, we demonstrate that existing whole genome sequencing (WGS) data contains ample non-human DNA sequences to reconstruct a molecular biomarker of latent EBV infection consistent with orthogonal phenotypes, including viral serology. Using the UK Biobank (n = 490,560) and All of Us (n = 245,394), we uncover reproducible complex trait associations that nominate latent blood-derived EBV DNA as a respiratory, autoimmune, and cardiovascular disease biomarker. Further, we evaluate the genetic determinants of persistent EBV DNA via genome-wide and exome-wide association studies, uncovering protein-altering variants from 147 genes. Single-cell and pathway-scale enrichment analyses implicate variable antigen processing and presentation as a primary genetic determinant of latent EBV persistence, with gene programs expressed in B cells and antigen-presenting cells. Using predicted viral epitope presentation affinities, we implicate genetic variation in MHC class II as a key modulator of EBV DNA persistence. Our analyses demonstrate how existing WGS data can derive novel molecular biomarkers, which may generalize to dozens of viruses comprising the blood virome1.

genetics↗

The genomic architecture of adaptation to larval malnutrition points to a trade-off with adult starvation resistance in Drosophila

Periods of nutrient shortage impose strong selection on animal populations. Experimental studies of genetic adaptation to nutrient shortage largely focus on resistance to acute starvation at adult stage; it is not clear how conclusions drawn from these studies extrapolate to other forms of nutritional stress. We studied the genomic signature of adaptation to chronic juvenile malnutrition in six populations of Drosophila melanogaster evolved for 150 generations on an extremely nutrient-poor larval diet. Comparison with control populations evolved on standard food revealed repeatable genomic differentiation between the two set of population, involving >3,000 candidate SNPs forming >100 independently evolving clusters. The candidate genomic regions were enriched in genes implicated in hormone, carbohydrate, and lipid metabolism, including some with known effects on fitness-related life-history traits. Rather than being close to fixation, a substantial fraction of candidate SNPs segregated at intermediate allele frequencies in all malnutrition-adapted populations. This, together with patterns of among-population variation in allele frequencies and estimates of Tajimas D, suggests that the poor diet results in balancing selection on some genomic regions. Our candidate genes for tolerance to larval malnutrition showed a high overlap with genes previously implicated in acute starvation resistance. However, adaptation to larval malnutrition in our study was associated with reduced tolerance to acute adult starvation. Thus, rather than reflecting synergy, the shared genomic architecture appears to mediate an evolutionary trade-off between tolerances to these two forms of nutritional stress.

evolutionary biology↗

Genetic analyses identify widespread sex-differential participation bias

Genetic association results are often interpreted with the assumption that study participation does not affect downstream analyses. Understanding the genetic basis of this participation bias is challenging as it requires the genotypes of unseen individuals. However, we demonstrate that it is possible to estimate comparative biases by performing GWAS contrasting one subgroup versus another. For example, we show that sex exhibits autosomal heritability in the presence of sex-differential participation bias. By performing a GWAS of sex in ~3.3 million males and females, we identify over 158 autosomal loci significantly associated with sex and highlight complex traits underpinning differences in study participation between sexes. For example, the body mass index (BMI) increasing allele at the FTO locus was observed at higher frequency in males compared to females (OR 1.02 [1.02-1.03], P=4.4x10-36). Finally, we demonstrate how these biases can potentially lead to incorrect inferences in downstream analyses and propose a conceptual framework for addressing such biases. Our findings highlight a new challenge that genetic studies may face as sample sizes continue to grow.

genetics↗

Male competition and the evolution of mating and life history traits in experimental populations of Aedes aegypti

Aedes aegypti is an important disease vector and a major target of reproductive control efforts. We manipulated the opportunity for sexual selection in populations of Ae. aegypti by controlling the number of males competing for a single female. Populations exposed to higher levels of male competition rapidly evolved higher male competitive mating success relative to populations evolved in the absence of competition, with an evolutionary response visible after only five generations. We also detected correlated evolution in other important mating and life history traits, such as acoustic signalling, fecundity and body size. Our results indicate that there is ample segregating variation for determinants of male mating competitiveness in wild populations and that increased male mating success trades-off with other important life history traits. The mating conditions imposed on laboratory-reared mosquitoes are likely a significant determinant of male mating success in populations destined for release.

evolutionary biology↗

Expanded genomic analyses for male voice-breaking highlights a shared phenotypic and genetic basis between puberty timing and hair colour

The timing of puberty is highly variable and has important consequences for long-term health. Most of our understanding of the genetic control of puberty timing is based on studies in women, as age at menarche is often recorded. Here, we report a multi-trait genome-wide association study for male puberty timing, based on recalled timing of voice breaking and facial hair, with an effective sample size of 205,354 men, nearly four-fold larger than previously reported. We identify 78 independent signals for male puberty timing, including 29 signals not previously associated with puberty in either sex. Novel mechanisms include an unexpected phenotypic and genetic link between puberty timing and natural hair colour, possibly reflecting common effects of pituitary hormones on puberty and pigmentation. Earlier male puberty timing is genetically correlated with several adverse health outcomes and, in Mendelian randomization analyses, shows causal relationships with higher risk of prostate cancer and shorter lifespan. These findings highlight the relationships between puberty timing and later health outcomes, and demonstrate the value of genetic studies of puberty timing in both sexes.

genomics↗

Extensive mitochondrial population structure and haplotype-specific phenotypic variation in the Drosophila Genetic Reference Panel

The Drosophila Genetic Reference Panel (DGRP) serves as a valuable resource to better understand the genetic landscapes underlying quantitative traits. However, such DGRP studies have so far only focused on nuclear genetic variants. To address this, we sequenced the mitochondrial genomes of >170 DGRP lines, identifying 229 variants including 21 indels and 7 frameshifts. We used our mitochondrial variation data to identify 12 genetically distinct mitochondrial haplotypes, thus revealing important population structure at the mitochondrial level. We further examined whether this population structure was reflected on the nuclear genome by screening for the presence of potential mito-nuclear genetic incompatibilities in the form of significant genotype ratio distortions (GRDs) between mitochondrial and nuclear variants. In total, we detected a remarkable 1,845 mito-nuclear GRDs, with the highest enrichment observed in a 40 kb region around the gene Sex-lethal (Sxl). Intriguingly, downstream phenotypic analyses did not uncover major fitness effects associated with these GRDs, suggesting that a large number of mito-nuclear GRDs may reflect population structure at the mitochondrial level rather than actual genomic incompatibilities. This is further supported by the GRD landscape showing particular large genomic regions associated with a single mitochondrial haplotype. Next, we explored the functional relevance of the detected mitochondrial haplotypes through an association analysis on a set of 259 assembled, non-correlating DGRP phenotypes. We found multiple significant associations with stress- and metabolism-related phenotypes, including food intake in males. We validated the latter observation by reciprocal swapping of mitochondrial genomes from high food intake DGRP lines to low food intake ones. In conclusion, our study uncovered important mitochondrial population structure and haplotype-specific metabolic variation in the DGRP, thus demonstrating the significance of incorporating mitochondrial haplotypes in geno-phenotype relationship studies.

genomics↗