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Slate, J.

Publications and source records attributed to Slate, J..

9 recordsLinked to original sources

Inbreeding depression by polygenic load following a severe population bottleneck

It is poorly understood how populations survive extreme bottlenecks despite severe inbreeding. We investigate the genomic architecture of inbreeding in the once critically endangered Seychelles warbler (Acrocephalus sechellensis) using 37 years of individual-based monitoring and 1.8 million SNPs. Linkage disequilibrium patterns reveal a historical effective population size of [~]270 that plummeted to [~]13 coinciding with human colonisation events of the Seychelles archipelago. Contemporary genomes are over one-third inbred from recent inbreeding measured by runs of homozygosity (ROH) formed since human colonisation of the Seychelles, 50 generations ago (mean FROH < 50 generations ago = 0.38), and we identify significant inbreeding depression across cross key fitness traits. On average, a 17.9% reduction in lifespan and a 15.1% reduction in lifetime offspring production were associated with each 10% increase in individual inbreeding. Genome-wide scans reveal this depression is caused by a polygenic load. Our results suggest that a history of small population size could have facilitated the selective purging of severe genetic load, while mildly deleterious alleles escaped selection via drift. A partitioned genetic load architecture potentially enabled species recovery despite the inbreeding depression that followed near-extinction.

evolutionary biology↗

A Seychelles warbler genomic toolkit

Understanding evolutionary processes is greatly facilitated by high-quality data on genetic variation. We report the development of a genomic toolkit for a recently bottlenecked, long-term studied species, the Seychelles warbler (Ptimerl dezil; Acrocephalus sechellensis). This toolkit comprises a reference genome assembled into 31 chromosomes, together with functional annotations and reference-panel-free imputation of whole-genome sequences from 1,935 individuals. The genomic data have been used to assign the sequenced individuals into a genetic pedigree. Individual genomic data are associated with a suite of phenotypic metadata, amassed from three decades of fieldwork in this closed, long-term monitored population. We compared sex and parentage assigned using the genomic data with the previously recorded sex and parentage metadata to identify and correct 41 sample DNA samples labelled with the wrong identity. This population resource enables a wide range of analyses, that include, but are not limited to phylogenetics, metabarcoding, recombination rates, linkage patterns, adaptation, heritability, demographic history, selection, and inbreeding estimates. We wish to encourage interest from researchers seeking to collaborate on future analyses and data collection. Overall, our methods demonstrate the potential of next generation sequencing and statistical tools to provide dense genomic datasets at large sample sizes for wild populations.

genomics↗

Adaptation to free-living drives loss of beneficial endosymbiosis through metabolic trade-offs

Symbioses are widespread (1) and underpin the function of diverse ecosystems (2-6), but their evolutionary stability is challenging to explain (7,8). Fitness trade-offs between contrasting intracellular and extracellular niches could act to stabilise endosymbioses because adaptation to either niche is predicted to reduce fitness in the alternate niche, thus reinforcing symbiosis (8,9). Here, we experimentally evolved four diverse Chlorella green algal endosymbionts of Paramecium bursaria to free-living conditions supplying either an amino acid, as provisioned by hosts (10,11), or nitrate, as available in freshwater (12), as the sole nitrogen source. Experimental algal populations adapted to free-living environments, generally increasing in population density and cellular chlorophyll content over time. In one of the four endosymbiont strains, adaptation to the nitrate free-living environment, but not the amino acid environments, drove the loss of fitness benefits to the host in reconstituted symbioses. This loss was not associated with reduced ability to grow on host-provisioned amino acids, nor lost ability to release the sugars provisioned to the host (10,13). Genome sequencing of evolved algal lines revealed genomic divergence between nitrate-adapted and amino acid-adapted lines, affecting genes involved with metabolic organisation and intracellular resource transport. Untargeted metabolomic profiling further showed extensive changes to membrane remodelling and turnover in N-evolved lines. Together, our data support a role for metabolic trade-offs driving divergence between contrasting intracellular and extracellular niches, with nitrogen as a key environmental axis driving divergence. Fitness trade-offs may, therefore, be a general, simple mechanism acting to reinforce symbiosis, contributing to evolutionary stability.

evolutionary biology↗

Genomic regions exhibiting divergent methylation patterns covary with loci associated with mate choice traits in a stick insect

Speciation involves the development of reproductive isolation between diverging populations. A potential key driver of reproductive isolation is mate choice, a behavioural mechanism that can limit gene flow based on divergence in signal traits. While the genetic basis of mating signal traits has been extensively studied, the contribution of epigenetic modifications to their variation remains underexplored, leaving the role of DNA methylation in mate choice unclear. Here, we focus on epigenetic variation and cuticular hydrocarbons (CHCs), the latter being chemical traits used for mate choice in insects. Specifically, we investigate the association between DNA methylation and regions associated with CHC variation in Timema cristinae stick insects. We integrate analyses of differentially methylated regions (DMRs) between individuals from different host-plant ecotypes with genomic sequencing and phenotypic data on CHCs. We find that DMRs are significantly enriched in genetic loci associated with CHCs, suggesting a non-random relationship between DNA methylation and loci associated with these signal traits. While further work is required to clarify causality, our results highlight the potential for epigenetic marks to be associated with traits involved in mate choice. Future studies should thus aim to establish causal links between DNA methylation and signal trait variation, which would clarify the contribution of methylation to mate choice, prezygotic isolation, and ultimately, speciation.

evolutionary biology↗

The genetic consequences of dispersal and immigration in a wild great tit population

Understanding how dispersal impacts the genetic makeup of populations is essential for predicting their responses to environmental change. Gene flow--via within-population dispersal and external immigration--shapes population health and evolutionary potential by boosting genetic diversity, but it can also counteract local adaptation. We investigate these processes in a population of great tits (Parus major) in Wytham Woods, United Kingdom. This system represents a large, continuous population of a vagile, widely distributed species. Using a comprehensive social pedigree alongside genomic data from two genomic datasets, one with 949 individuals genotyped at ~600,000 SNPs and another with 2,644 individuals at ~10,000 SNPs, we observe some spatial genetic structure largely driven by the spatial and temporal clustering of close kin. We quantify how temporally persistent this pattern is and find similar levels of decay of relatedness with distance across years, without a consistent genetic basis, which is frequently renewed due to high population turnover. Immigrants make up a substantial portion of the breeding population, yet are often assumed to be genetically distinct, unrelated, and outbred--assumptions that can bias population inferences. We show that immigrants are indeed outbred, as are local birds; have fewer close relatives within the population, and are less likely to be related to their neighbours than locally born birds. Despite low FST and no clear genome-wide population structure, immigrants and locals can be distinguished above chance using a Random Forest classifier trained on SNP data. Our study highlights the complex interplay between dispersal, population turnover and spatial population structure, and suggests that great tits in Wytham Woods experience substantial gene flow within the population and from immigrants, maintaining high genetic diversity and reducing the possibility of local adaptation at this spatial scale.

evolutionary biology↗

Ecology not genetics explains correlated trait divergence during speciation

The formation of new species often involves the correlated divergence of multiple traits and genetic regions. However, the mechanisms by which such trait covariation builds up remain poorly understood. In this context, we consider two non-exclusive hypotheses. First, genetic covariance between traits can cause divergent selection on one trait to promote population divergence in correlated traits (a genetic covariation hypothesis). Second, correlated environmental pressures can generate selection on multiple traits, facilitating the evolution of trait complexes (an environmental covariation hypothesis). Here, we test these hypotheses using cryptic coloration (controlled by an incipient supergene) and chemical traits (i.e., cuticular hydrocarbons, CHCs) involved in desiccation resistance and mate choice in Timema cristinae stick insects. We first demonstrate that population divergence in color-pattern is correlated with divergence in some (but not all) CHC traits. We show that when correlated population divergence does occur, it is unlikely to be explained by genetic covariation because within-population genetic covariance between color-pattern and CHCs traits is weak. In contrast, we find that correlated variation in climate and host plant likely generates selection jointly on color-pattern and some CHC traits. This supports the environmental covariation hypothesis, likely via the effects of two correlated environmental axes selecting on different traits. Finally, we provide evidence that misalignment between natural and sexual selection also contributes to patterns of correlated trait divergence. Our results shed light into transitions between phases of speciation by showing that environmental factors can promote population divergence in trait complexes, even without strong genetic covariance.

evolutionary biology↗

The ghost of selection past: evolution and conservation relevance of the kakapo color polymorphism

The information contained in population genomic data can tell us much about the past ecology and evolution of species. We leveraged detailed phenotypic and genomic data of nearly all living k[a]k[a]p[o] to understand the evolution of its remarkable feather color polymorphism. The k[a]k[a]p[o] is an endangered and culturally significant parrot endemic to Aotearoa New Zealand, and the green and olive feather colorations are present at similar frequencies in the population. The presence of such a neatly balanced color polymorphism is remarkable because the entire population currently numbers less than 250 birds, which means it has been exposed to severe genetic drift. We dissected the color phenotype, demonstrating that the two colors differ in their light reflectance patterns due to differential feather structure. We used quantitative genomics methods to identify two genetic variants whose epistatic interaction can fully explain the species color phenotype. Our genomic forward simulations show that balancing selection might have been pivotal to establish the polymorphism in the ancestrally large population, and to maintain it during population declines that involved a severe bottleneck. We hypothesize that an extinct apex predator was the likely agent of balancing selection, making the color polymorphism in the k[a]k[a]p[o] a "ghost of selection past".

genomics↗

Using genomic prediction to detect microevolutionary change of a quantitative trait

Detecting microevolutionary responses to natural selection by observing temporal changes in individual breeding values is challenging. The collection of suitable datasets can take many years and disentangling the contributions of the environment and genetics to phenotypic change is not trivial. Furthermore, pedigree-based methods of obtaining individual breeding values have known biases. Here, we apply a genomic prediction approach to estimate breeding values of adult weight in a 35-year dataset of Soay sheep (Ovis aries). During the study period adult body weight decreased, but the underlying genetic component of body weight increased, at a rate that is unlikely to be attributable to genetic drift. Thus cryptic microevolution of greater adult body weight has probably occurred. Using genomic prediction to study microevolution in wild populations can remove the requirement for pedigree data, potentially opening up new study systems for similar research.

evolutionary biology↗

Genomic prediction in the wild: A case study in Soay sheep

Genomic prediction, the technique whereby an individuals genetic component of their phenotype is estimated from its genome, has revolutionised animal and plant breeding and medical genetics. However, despite being first introduced nearly two decades ago, it has hardly been adopted by the evolutionary genetics community studying wild organisms. Here, genomic prediction is performed on eight traits in a wild population of Soay sheep. The population has been the focus of a >30 year evolutionary ecology study and there is already considerable understanding of the genetic architecture of the focal Mendelian and quantitative traits. We show that the accuracy of genomic prediction is high for all traits, but especially those with loci of large effect segregating. Five different methods are compared, and the two methods that can accommodate zero-effect and large-effect loci in the same model tend to perform best. If the accuracy of genomic prediction is similar in other wild populations, then there is a real opportunity for pedigree-free molecular quantitative genetics research to be enabled in many more wild populations; currently the literature is dominated by studies that have required decades of field data collection to generate sufficiently deep pedigrees. Finally, some of the potential applications of genomic prediction in wild populations are discussed.

evolutionary biology↗