Biology subjects

Richards, E. J.

Publications and source records attributed to Richards, E. J..

9 recordsLinked to original sources

bioRxiv2026

Cave evolution on repeat: reuse of the same genomic regions across lineages but not across traits in Astyanax mexicanus

Similar traits repeatedly evolve across independent populations in response to similar environmental conditions. For many repeatedly evolved traits it is unknown if populations evolve similar traits through the same or different genetic mechanisms. To address this question, we leveraged the Mexican tetra fish, Astyanax mexicanus, which has evolved repeatedly through altering many traits including reduced sleep duration, eye degeneration, and metabolic shifts to accommodate limited nutrient availability. We defined whether shared or independent genetic architecture govern the repeated evolution of sleep loss, increased food consumption, early onset adipose deposition, and eye loss in different evolutionary origins of the cavefish phenotype by using Quantitative Trait Locus (QTL) mapping across three cave x surface F2 mapping populations. We found that, among the traits evaluated, eye loss exhibits the most genetic repeatability, with [~]43% of QTL shared across lineages. Sleep loss and metabolic traits (i.e., feeding, adiposity) were genetically less repeatable, with only [~]25-33% of QTL shared across lineages. Next, we explored whether QTL for metabolism, eye loss, and sleep traits in cavefish co-localize in the cavefish genome and could be inherited together to facilitate potential cavefish adaptation. Although these traits have repeatedly co-evolved in cave populations, we did not find evidence for extensive genetic linkage among them. Overall, we found that genetic repeatability is a common feature in the repeated evolution of cave traits, the extent of genetic repeatability varies across cave traits, and that there is little evidence for widespread co-localization of sleep, eye loss, and metabolic traits within the genome. SummaryIndependent populations that evolve similar traits in response to similar environmental conditions provide us with natural replicates for studying what constrains evolutionary change. Iconic examples of repeated trait evolution often involve repeated mutations in the same genes, suggesting there are limits on the type of genes and mutations that can contribute to phenotypic evolution. Here we conduct a multi-trait, multi-population QTL analysis for similar eye loss, sleep loss and metabolic shifts across two lineages of Astyanax mexicanus. Genetic repeatability is present for most traits, but its extent is highly trait dependent and occurs at the level of genomic regions rather than specific genes, highlighting the mosaic of constraint and flexibility involved in genetic repeatability.

evolutionary biology↗

bioRxiv2024

Structural diversity and distribution of NMCP-class nuclear lamina proteins in streptophytic algae

Nuclear Matrix Constituent Proteins (NMCPs) in plants function like animal lamins, providing the structural foundation of the nuclear lamina and regulating nuclear organization and morphology. Although they are well-characterized in angiosperms, the presence and structure of NMCPs in more distantly related species, such as streptophytic algae, are relatively unknown. The rapid evolution of NMCPs throughout the plant lineage has caused a divergence in protein sequence that makes similarity-based searches less effective. Structural features are more likely to be conserved compared to primary amino acid sequence; therefore, we developed a filtration protocol to search for diverged NMCPs based on four physical characteristics: intrinsically disordered content, isoelectric point, number of amino acids, and the presence of a central coiled-coil domain. By setting parameters to recognize the properties of bona fide NMCP proteins in angiosperms, we filtered eight complete proteomes from streptophytic algae species and identified strong NMCP candidates in six taxa in the Classes Zygnematophyceae, Charophyceae, and Klebsormidophyceae. Through analysis of these proteins, we observed structural variance in domain size between NMCPs in algae and land plants, as well as a single block of amino acid conservation. Our analysis indicates that NMCPs are absent in the Mesostigmatophyceae. The presence versus absence of NMCP proteins does not correlate with the distribution of different forms of mitosis (e.g., closed/semi-closed/open) but does correspond to the transition from unicellularity to multicellularity in the streptophytic algae, suggesting that an NMCP-based nucleoskeleton plays important roles in supporting cell-to-cell interactions. SIGNIFICANCE STATEMENTAll eukaryotic organisms contain a membrane-bound nucleus, which holds a cells DNA, but plants and animals have distinct sets of proteins that make up the mesh-like scaffold inside the nucleus (i.e., nuclear lamina) that is essential for structural integrity and organization. Nonetheless, the major nuclear lamina proteins in plants and animals share structural features, and we exploited these characteristics to identify a key class of nuclear lamina proteins in streptophytic algae, allowing us to chart the distribution of these proteins across photosynthetic organisms and to gain insight into the evolution of nuclear organization. Our results indicate that the major class of nuclear lamina protein in plants evolved independently from structurally similar nuclear lamina proteins in animals.

plant biology↗

bioRxiv2024

Loci associated with cave-derived traits concentrate in specific regions of the Mexican cavefish genome

A major goal of modern evolutionary biology is connecting phenotypic evolution with its underlying genetic basis. The Mexican cavefish (Astyanax mexicanus), a characin fish species comprised of a surface ecotype and a cave-derived ecotype, is well suited as a model to study the genetic mechanisms underlying adaptation to extreme environments. Here we map 206 previously published quantitative trait loci (QTL) for cave-derived traits in A. mexicanus to the newest version of the surface fish genome assembly, AstMex3. This analysis revealed that QTL cluster in the genome more than expected by chance, and this clustering is not explained by the distribution of genes in the genome. To investigate whether certain characteristics of the genome facilitate phenotypic evolution, we tested whether genomic characteristics, such as highly mutagenic CpG sites, are reliable predictors of the sites of trait evolution but did not find any significant trends. Finally, we combined the QTL map with previously collected expression and selection data to identify a list of 36 candidate genes that may underlie the repeated evolution of cave phenotypes, including rgrb which is predicted to be involved in phototransduction. We found this gene has disrupted exons in all non-hybrid cave populations but intact reading frames in surface fish. Overall, our results suggest specific "evolutionary hotspots" in the genome may play significant roles in driving adaptation to the cave environment in Astyanax mexicanus and demonstrate how this compiled dataset can facilitate our understanding of the genetic basis of repeated evolution in the Mexican cavefish.

evolutionary biology↗

bioRxiv2023

Discovery of a new craniofacial gene influencing adaptive phenotypes in a non-model pupfish radiation

Understanding the genetic basis of novel adaptations in new species is a fundamental question in biology that also provides an opportunity to uncover new genes and regulatory networks with potential clinical relevance. Here we demonstrate a new role for galr2 in vertebrate craniofacial development using an adaptive radiation of trophic specialist pupfishes endemic to San Salvador Island in the Bahamas. We confirmed the loss of a putative Sry transcription factor binding site in the upstream region of galr2 in scale-eating pupfish and found significant spatial differences in galr2 expression among pupfish species in Meckels cartilage and premaxilla using in situ hybridization chain reaction (HCR). We then experimentally demonstrated a novel function for Galr2 in craniofacial development and jaw elongation by exposing embryos to drugs that inhibit Galr2 activity. Galr2-inhibition reduced Meckels cartilage length and increased chondrocyte density in both trophic specialists but not in the generalist genetic background. We propose a mechanism for jaw elongation in scale-eaters based on the reduced expression of galr2 due to the loss of a putative Sry binding site. Fewer Galr2 receptors in the scale-eater Meckels cartilage may result in their enlarged jaw lengths as adults by limiting opportunities for a postulated Galr2 agonist to bind to these receptors during development. Our findings illustrate the growing utility of linking candidate adaptive SNPs in non-model systems with highly divergent phenotypes to novel vertebrate gene functions.

developmental biology↗

bioRxiv2022

Selection-driven trait loss in independently evolved cavefish populations

Predicting the outcome of evolution is a central goal of modern biology, yet, determining the relative contributions of deterministic events (i.e., selection) and stochastic events (i.e., drift and mutation) to the evolutionary process remains a major challenge. Systems where the same traits have evolved repeatedly provide natural replication that can be leveraged to study the predictability of molecular evolution and the genetic basis of adaptation. Although mutational screens in the laboratory have demonstrated that a diversity of genetic mutations can produce phenocopies of one another, in natural systems, similar genetic changes frequently underly the evolution of phenotypes across independent lineages. This suggests a substantial role for constraint and determinism in evolution and supports the notion that there may be characteristics which make certain mutations more likely to contribute to phenotypic evolution. Here we use large-scale whole genome resequencing in the Mexican tetra, Astyanax mexicanus, to demonstrate that selection has played a primary role in repeated evolution of both trait loss and trait enhancement across independent cave lineages. We identify candidate genes underlying repeated adaptation to caves and infer the mode of repeated evolution, revealing that selection on standing genetic variation and de novo mutations both contribute substantially to repeated adaptation. Finally, we show that genes with evidence of repeated evolution have significantly longer coding regions compared to the rest of the genome, and this effect is most pronounced in genes evolving convergently via independent mutations. Importantly, our findings provide the first empirical support for the hypothesis that genes with larger mutational targets are more likely to be the substrate of repeated evolution and indicate that features of the novel cave environment may impact the rate at which mutations occur.

evolutionary biology↗

bioRxiv2020

Major stages of vertebrate adaptive radiation are assembled from a disparate spatiotemporal landscape

To investigate the origins and stages of vertebrate adaptive radiation, we reconstructed the spatial and temporal histories of genetic variants underlying major phenotypic axes of diversification from the genomes of 202 Caribbean pupfishes. Ancient standing variation from disparate spatial sources was reassembled into new combinations which are under strong selection for adaptation to novel trophic niches on only a single island throughout the Caribbean. This occurred in three stages: first, standing variation associated with feeding behavior swept, then standing variation regulating craniofacial development and pigmentation, and finally de novo variation for craniofacial development. Our results provide clear support for two longstanding hypotheses about adaptive radiation and demonstrate how ancient alleles maintained for millennia in distinct environmental refugia can be assembled into new adaptive combinations. One Sentence SummaryAncient origins of adaptive radiation

evolutionary biology↗

bioRxiv2017

Speciation in sympatry with ongoing secondary gene flow and an olfactory trigger in a radiation of Cameroon cichlids

Whether speciation can happen in the absence of geographical barriers and if so, under which conditions, is a fundamental question in our understanding of the evolution of new species. Among candidates for sympatric speciation, Cameroon crater lake cichlid radiations have been considered the most compelling. However, it was recently shown that a more complex scenario than a single colonization followed by isolation underlies these radiations. Here, we perform a detailed investigation of the speciation history of a radiation of Coptodon cichlids from Lake Ejagham using whole-genome sequencing data. The existence of the Lake Ejagham Coptodon radiation is remarkable since this 0.5 km2 lake offers limited scope for divergence across a shallow depth gradient, disruptive selection is weak, the species are sexually monochromatic, yet assortative mating is strong. We infer that Lake Ejagham was colonized by Coptodon cichlids almost as soon as it came into existence 9,000 years ago, yet speciation events occurred only in the last 1,000-2,000 years. We show that secondary gene flow from a nearby riverine species has been ongoing, into ancestral as well as extant Lake Ejagham lineages, and we identify and date river-to-lake admixture blocks. One of these contains a cluster of olfactory receptor genes that introgressed close to the time of the first speciation event and coincides with a higher overall rate of admixture into the recipient lineages. Olfactory signaling is a key component of mate choice and species recognition in cichlids. A functional role for this introgression event is consistent with previous findings that assortative mating appears much stronger than ecological divergence in Ejagham Coptodon. We conclude that speciation in this radiation took place in sympatry, yet may have benefited from ongoing riverine gene flow.\n\nAuthor SummaryDespite an active search for empirical examples and much theoretical work, sympatric speciation remains one of the most controversial ideas in evolutionary biology. While a host of examples have been described in the last few decades, more recent results have shown that several of the most convincing systems have not evolved in complete isolation from allopatric populations after all. By itself, documenting the occurrence of secondary gene flow is not sufficient to reject the hypothesis of sympatric speciation, since speciation can still be considered sympatric if gene flow did not contribute significantly to the build-up of reproductive isolation. One way forward is to use genomic data to infer where, when and into which lineages gene flow occurred, and identify the regions of the genome that experienced admixture. In this study, we use whole-genome sequencing to examine one of the cichlid radiations from a small isolated Cameroon lake, which have long been the flagship example of sympatric speciation. We show that gene flow from a riverine species into the lake has been ongoing during the history of the radiation. In line with this, we infer that the lake was colonized very soon after it was formed, and argue that Lake Ejagham is not as isolated as previously assumed. The magnitude of secondary gene flow was relatively even across Lake Ejagham lineages, yet with some evidence for differential admixture, most notably before the first speciation event into the C. deckerti and C. ejagham lineage. Among the sequences that were introgressed into this lineage is a cluster of olfactory receptor genes, which may have facilitated speciation by promoting sexual isolation between incipient species, consistent with previous findings that sexual isolation appears to be stronger than ecological isolation in Ejagham Coptodon. We conclude that speciation in this radiation took place in sympatry, yet may have benefited from ongoing riverine gene flow.

evolutionary biology↗

bioRxiv2017

Unexpected variation across mitochondrial gene trees and evidence for systematic error: How much gene tree variation is biological?

The use of large genomic datasets in phylogenetics has highlighted extensive topological variation across genes. Much of this discordance is assumed to result from biological processes. However, variation among gene trees can also be a consequence of systematic error driven by poor model fit, and the relative importance of these biological versus methodological factors in explaining gene tree variation is a major unresolved question in phylogenetics. Using mitochondrial genomes to control for biological causes of gene tree variation, we estimate the extent of gene tree discordance driven by systematic error and employ posterior prediction to highlight the role of model fit. We find that the amount of discordance among mitochondrial gene trees is similar to the amount of discordance found in other studies that assume only biological causes of variation. This similarity suggests that the role of systematic error in generating gene tree variation is underappreciated and that critical evaluation of the fit between assumed models and the data used for inference is important for the resolution of unresolved phylogenetic questions.

evolutionary biology↗

bioRxiv2017

Adaptive introgression from distant Caribbean islands contributed to the diversification of a microendemic radiation of trophic specialist pupfishes

Rapid diversification often involves complex histories of gene flow that leave variable and conflicting signatures of evolutionary relatedness across the genome. Identifying the extent and source of variation in these evolutionary relationships can provide insight into the evolutionary mechanisms involved in rapid radiations. Here we compare the discordant evolutionary relationships associated with species phenotypes across 42 whole genomes from a sympatric adaptive radiation of Cyprinodon pupfishes endemic to San Salvador Island, Bahamas and several outgroup pupfish species in order to understand the rarity of these trophic specialists within the larger radiation of Cyprinodon. 82% of the genome depicts close evolutionary relationships among the San Salvador Island species reflecting their geographic proximity, but the vast majority of the fixed variants between the specialist species lie in regions with discordant topologies. These regions include signatures of selective sweeps and adaptive introgression from neighboring islands into each of the specialist species. Hard selective sweeps of genetic variation on San Salvador contributed 10-fold more to divergence between specialist species within the radiation than adaptive introgression of Caribbean genetic variation; however, some of these introgressed regions from distant islands were associated with the primary axis of oral jaw divergence within the radiation. For example, standing variation in a proto-oncogene (ski) known to have effects on jaw size introgressed into one San Salvador specialist from an island 300 km away. The complex emerging picture of the origins of adaptive radiation on San Salvador indicates that multiple sources of genetic variation contributed to the adaptive phenotypes of novel trophic specialists on the island. Our findings suggest that a suite of factors, including rare adaptive introgression, may also be required to trigger adaptive radiation in the presence of ecological opportunity.\n\nAuthor summaryGroups of closely related species can rapidly evolve to occupy diverse ecological roles, but the ecological and genetic conditions that trigger this diversification are still highly debated. We examine patterns of molecular evolution across the genomes of a rapid radiation of pupfishes that includes two trophic specialists. Despite apparently widespread ecological opportunities and gene flow across the Caribbean, this radiation is endemic to a single Bahamian Island. Using the whole genomes of 42 pupfish we find evidence of extensive and previously unexpected variation in evolutionary relatedness among Caribbean pupfish. Two sources of genetic variation have contributed to the adaptive diversification of complex phenotypes in this system: selective sweeps of genetic variation from across the Caribbean that was brought into San Salvador through hybridization and genetic variation found on San Salvador. While genetic variation from San Salvador appears to be relatively more common in the divergence observed among specialists, hybridization probably played an important role in the evolution of the complex phenotypes as well. Our findings that multiple sources of genetic variation contribute to the San Salvador radiation suggest that a complex suite of factors, including hybridization with other species, may be required to trigger adaptive radiation in the presence of ecological opportunity.

evolutionary biology↗