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Results for “Evolutionary Biology”

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bioRxiv2018

Detection of adaptive divergence in populations of the stream mayfly Ephemera strigata with machine learning

Adaptive divergence is a key mechanism shaping the genetic variation of natural populations. A central question linking ecology with evolutionary biology concerns the role of environmental heterogeneity in determining adaptive divergence among local populations within a species. In this study, we examined adaptive the divergence among populations of the stream mayfly Ephemera strigata in the Natori River Basin in northeastern Japan. We used a genome scanning approach to detect candidate loci under selection and then applied a machine learning method (i.e. Random Forest) and traditional distance-based redundancy analysis (dbRDA) to examine relationships between environmental factors and adaptive divergence at non-neutral loci. We also assessed spatial autocorrelation at neutral loci to quantify the dispersal ability of E. strigata. Our main findings were as follows: 1) random forest shows a higher resolution than traditional statistical analysis for detecting adaptive divergence; 2) separating markers into neutral and non-neutral loci provides insights into genetic diversity, local adaptation and dispersal ability and 3) E. strigata shows altitudinal adaptive divergence among the populations in the Natori River Basin.

evolutionary biology↗

bioRxiv2014

SINGLE NUCLEOTIDE POLYMORPHISMS SHED LIGHT ON CORRELATIONS BETWEEN ENVIRONMENTAL VARIABLES AND ADAPTIVE GENETIC DIVERGENCE AMONG POPULATIONS IN ONCORHYNCHUS KETA

Identifying the genetic and ecological basis of adaptation is of immense importance in evolutionary biology. In our study, we applied a panel of 58 biallelic single nucleotide polymorphisms (SNPs) for the economically and culturally important salmonid Oncorhynchus keta. Samples included 4164 individuals from 43 populations ranging from Coastal Western Alaska to southern British Colombia and northern Washington. Signatures of natural selection were detected by identifying seven outlier loci using two independent approaches: one based on outlier detection and another based on environmental correlations. Evidence of divergent selection at two candidate SNP loci, Oke_RFC2-168 and Oke_MARCKS-362, indicates significant environmental correlations, particularly with the number of frost-free days (NFFD). Important associations found between environmental variables and outlier loci indicate that those environmental variables could be the major driving forces of allele frequency divergence at the candidate loci. NFFD, in particular, may play an important adaptive role in shaping genetic variation in O. keta. Correlations between divergent selection and local environmental variables will help shed light on processes of natural selection and molecular adaptation to local environmental conditions.

Evolutionary Biology↗

bioRxiv2018

Bayesian and likelihood placement of fossils on phylogenies from quantitative morphometrics

AO_SCPLOWBSTRACTC_SCPLOWJointly developing a comprehensive tree of life from living and fossil taxa has long been a fundamental goal in evolutionary biology. One major challenge has stemmed from difficulties in merging evidence from extant and extinct organisms. While these efforts have resulted in varying stages of synthesis, they have been hindered by their dependence on qualitative descriptions of morphology. Though rarely applied to phylogenetic inference, traditional and geometric morphometric data can improve these issues by generating more rigorous ways to quantify variation in morphological structures. They may also facilitate the rapid and objective aggregation of large morphological datasets. I describe a new Bayesian method that leverages quantitative trait data to reconstruct the positions of fossil taxa on fixed reference trees composed of extant taxa. Unlike most formulations of phylogenetic Brownian motion models, this method expresses branch lengths in units of morphological disparity, suggesting a new framework through which to construct Bayesian node calibration priors for molecular dating and explore comparative patterns in morphological disparity. I am hopeful that the approach described here will help to facilitate a deeper integration of neo- and paleontological data to move morphological phylogenetics further into the genomic era.

evolutionary biology↗

bioRxiv2018

Repeated inversions at the pannier intron drive diversification of intraspecific colour patterns of ladybird beetles

How genetic information is modified to generate phenotypic variation within a species is one of the central questions in evolutionary biology. Here we focus on the striking intraspecific diversity of more than 200 aposematic elytral (forewing) colour patterns of the multicoloured Asian ladybird beetle, Harmonia axyridis, which is regulated by a tightly linked genetic locus h. Our loss-of-function analyses, genetic association studies, de novo genome assemblies, and gene expression data reveal that the GATA transcription factor gene pannier is the major regulatory gene located at the h locus, and suggest that repeated inversions and cis-regulatory modifications at pannier led to the expansion of colour pattern variation in H. axyridis. Moreover, we show that the colour patterning function of pannier is conserved in the seven spotted ladybird beetle, Coccinella septempunctata, suggesting that H. axyridis extraordinary intra-specific variation may have arisen from ancient modifications in a conserved elytral colour patterning mechanisms in ladybird beetles.

evolutionary biology↗

bioRxiv2016

The Phenotypic, Genotypic, & Environmental Drivers of Local Adaptation to a Harsh Granite Outcrop Environment in Mimulus

A primary goal in evolutionary biology is to understand which environmental variables and traits drive adaptation to harsh environments. This is difficult since many traits evolve simultaneously as populations or species diverge. Here we investigate the ecological variables and traits that underlie Mimulus laciniatus adaptation to granite outcrops compared to its sympatric, mesic-adapted progenitor M. guttatus. We use fine scale measurements of soil moisture and herbivory to examine differences in selective forces between the species habitats, and measure selection on flowering time, flower size, plant height, and leaf shape in a reciprocal transplant using M. laciniatus x M. guttatus F4 hybrids. We find that differences in drought & herbivory drive survival differences between habitats, that M. laciniatus and M. guttatus are each better adapted to their native habitat, and differential habitat selection on flowering time, plant stature, and leaf shape. We conclude that while early flowering time, small stature, and lobed leaf shape underlie plant fitness in M. laciniatus seasonally dry environment, increased plant size is advantageous in a competitive mesic environment replete with herbivores like M. guttatus.

evolutionary biology↗

bioRxiv2017

Parallel radiations of Cremastosperma and Mosannona (Annonaceae), tropical rainforest trees tracking Neogene upheaval of the South American continent

This preprint has been reviewed and recommended by Peer Community In Evolutionary Biology (http://dx.doi.org/10.24072/pci.evolbiol.100033). Much of the immense present day biological diversity of Neotropical rainforests originated from the Miocene onwards, a period of geological and ecological upheaval in South America. We assess the impact of the Andean orogeny, drainage of lake Pebas, and closure of the Panama Isthmus on two clades of trees (Cremastosperma, c. 31 spp.; and Mosannona, c. 14 spp.; both Annonaceae) found in humid forest distributed across the transition zones between the Andes and Western (lowland) Amazonia and between Central and South America. We inferred phylogenies based on c. 80% of recognised species of each clade using plastid and nuclear encoded sequence markers, revealing similar patterns of geographically restricted clades. Using molecular dating we showed that diversifications in the different areas occurred in parallel, with timing consistent with Andean vicariance and Central American geodispersal. In apparent contradiction of high dispersal abilities of rainforest trees, Cremastosperma clades within Amazonia are also geographically restricted, with a southern/montane clade that appears to have diversified along the foothills of the Andes sister to one of more northern/lowland species that diversified in a region once inundated by lake Pebas. Ecological niche modelling approaches show phylogenetically conserved niche differentiation, particularly within Cremastosperma. Niche similarity and recent common ancestry of Amazon and Guianan Mosannona species contrasts with dissimilar niches and more distant ancestry of Amazon, Venezuelan and Guianan species of Cremastosperma suggesting that this element of the similar patterns of disjunct distributions in the two genera is instead a biogeographic parallelism, with differing origins. The results provide further independent evidence for the importance of the Andean orogeny, the drainage of Lake Pebas, and the formation of links between South and Central America in the evolutionary history of Neotropical lowland rainforest trees.

evolutionary biology↗

bioRxiv2018

Landscape permeability and individual variation in a dispersal-linked gene jointly determine genetic structure in the Glanville fritillary butterfly

There is now clear evidence that species across a broad range of taxa harbour extensive heritable variation in dispersal. While studies suggest that this variation can facilitate demographic outcomes such as range expansion and invasions, few have considered the consequences of intraspecific variation in dispersal for the maintenance and distribution of genetic variation across fragmented landscapes. Here we examine how landscape characteristics and individual variation in dispersal combine to predict genetic structure using genomic and spatial data from the Glanville fritillary butterfly. We used linear and latent factor mixed models to identify the landscape features that best predict spatial sorting of alleles in the dispersal-related gene phosphoglucose isomerase (Pgi). We next used structural equation modeling to test if variation in Pgi mediated gene flow as measured by Fst at putatively neutral loci. In a year when the population was expanding following a large decline, individuals with a genotype associated with greater dispersal ability were found at significantly higher frequencies in populations isolated by water and forest, and these populations showed lower levels of genetic differentiation at neutral loci. These relationships disappeared in the next year when metapopulation density was high, suggesting that the effects of individual variation are context dependent. Together our results highlight that 1) more complex aspects of landscape structure beyond just the configuration of habitat can be important for maintaining spatial variation in dispersal traits, and 2) that individual variation in dispersal plays a key role in maintaining genetic variation across fragmented landscapes.\n\nImpact summaryUnderstanding how fragmentation affects dispersal and gene flow across human-modified landscapes has long been a goal in evolutionary biology. It is typically assumed that individuals of the same species respond to the landscape in the same way, however growing evidence suggests that individuals can vary considerably in their dispersal traits. While the effects of this individual dispersal variation on range expansions and invasions have been well-characterized, knowledge of how it might mediate genetic responses to landscape fragmentation are almost entirely lacking. Here we demonstrate that individual variation in dispersal is key to the maintenance of genetic variation during a population expansion following a large decline in a butterfly metapopulation. We further show that spatial variation in dispersal is not maintained by the configuration of habitat patches alone, but by a more complex genotype-environment interaction involving the landscape matrix (i.e. landscape features found between habitat patches). This challenges the simplified landscape representations typically used in studies of dispersal evolution that ignore heterogeneity in the landscape matrix. More broadly, our results highlight the interplay of adaptive and neutral processes across fragmented landscapes, suggesting that an understanding of species vulnerability to landscape fragmentation requires consideration of both.

evolutionary biology↗

bioRxiv2015

The origins of a novel butterfly wing patterning gene from within a family of conserved cell cycle regulators

A major challenge in evolutionary biology is to understand the origins of novel structures. The wing patterns of butterflies and moths are derived phenotypes unique to the Lepidoptera. Here we identify a gene that we name poikilomousa (poik), which regulates colour pattern switches in the mimetic Heliconius butterflies. Strong associations between phenotypic variation and DNA sequence variation are seen in three different Heliconius species, in addition to associations between gene expression and colour pattern. Colour pattern variants are also associated with differences in splicing of poik transcripts. poik is a member of the conserved fizzy family of cell cycle regulators. It belongs to a faster evolving subfamily, the closest functionally characterised orthologue being the cortex gene in Drosophila, a female germ-line specific protein involved in meiosis. poik appears to have adopted a novel function in the Lepidoptera and become a major target for natural selection acting on colour and pattern variation in this group.

Evolutionary Biology↗

bioRxiv2018

Efficiently inferring the demographic history of many populations with allele count data

The sample frequency spectrum (SFS), or histogram of allele counts, is an important summary statistic in evolutionary biology, and is often used to infer the history of population size changes, migrations, and other demographic events affecting a set of populations. The expected multipopulation SFS under a given demographic model can be efficiently computed when the populations in the model are related by a tree, scaling to hundreds of populations. Admixture, back-migration, and introgression are common natural processes that violate the assumption of a tree-like population history, however, and until now the expected SFS could be computed for only a handful of populations when the demographic history is not a tree. In this article, we present a new method for efficiently computing the expected SFS and linear functionals of it, for demographies described by general directed acyclic graphs. This method can scale to more populations than previously possible for complex demographic histories including admixture. We apply our method to an 8-population SFS to estimate the timing and strength of a proposed \"basal Eurasian\" admixture event in human history. We implement and release our method in a new open-source software package momi2.

evolutionary biology↗

bioRxiv2015

Population genomic scans reveal novel genes underlie convergent flowering time evolution in the introduced range of Arabidopsis thaliana

A long-standing question in evolutionary biology is whether the evolution of convergent phenotypes results from selection on the same heritable genetic components. Using whole genome sequencing and genome scans, we tested whether the evolution of parallel longitudinal flowering time clines in the native and introduced ranges of Arabidopsis thaliana has a similar genetic basis. We found that common variants of large effect on flowering time in the native range do not appear to have been under recent strong selection in the introduced range. Genes in regions of the genome that are under selection for flowering time are also not enriched for functions related to development or environmental sensing. We instead identified a set of 53 new candidate genes putatively linked to the evolution of flowering time in the species introduced range. A high degree of conditional neutrality of flowering time variants between the native and introduced range may preclude parallel evolution at the level of genes. Overall, neither gene pleiotropy nor available standing genetic variation appears to have restricted the evolution of flowering time in the introduced range to high frequency variants from the native range or to known flowering time pathway genes.

Evolutionary Biology↗

bioRxiv2017

Diminishing returns of inoculum size on the rate of a plant RNA virus evolution

Understanding how genetic drift, mutation and selection interplay in determining the evolutionary fate of populations is one of the central questions of Evolutionary Biology. Theory predicts that by increasing the number of coexisting beneficial alleles in a population beyond some point does not necessarily translates into an acceleration in the rate of evolution. This diminishing-returns effect of beneficial genetic variability in microbial asexual populations is known as clonal interference. Clonal interference has been shown to operate in experimental populations of animal RNA viruses replicating in cell cultures. Here we carried out experiments to test whether a similar diminishing-returns of population size on the rate of adaptation exists for a plant RNA virus infecting real multicellular hosts. We have performed evolution experiments with tobacco etch potyvirus in two hosts, the natural and a novel one, at different inoculation sizes and estimated the rates of evolution for two phenotypic fitness-related traits. Firstly, we found that evolution proceeds faster in the novel than in the original host. Secondly, we found the predicted diminishing-returns effect of inoculum size on the rate of evolution for one of the fitness traits, but not for the other, which suggests that selection operates differently on each trait.

evolutionary biology↗

bioRxiv2017

Unique genetic variants underlie parallel gene expression within a young adaptive radiation despite specialization on highly divergent resources

Parallel evolution of gene expression commonly underlies convergent niche specialization, but parallel changes in expression could also underlie divergent specialization. We investigated divergence in gene expression and whole-genome genetic variation across three sympatric Cyprinodon pupfishes endemic to San Salvador Island, Bahamas. This recent radiation consists of a generalist and two derived specialists adapted to novel niches - a scale-eater and a snail-eater. We sampled total mRNA from all three species at two early developmental stages and compared gene expression with whole-genome genetic differentiation among all three species in 42 resequenced genomes. 80% of genes that were differentially expressed between snail-eaters and generalists were up or downregulated in the same direction between scale-eaters and generalists; however, there were no fixed variants shared between species underlying these parallel changes in expression. Genes showing parallel evolution of expression were enriched for effects on metabolic processes, whereas genes showing divergent expression were enriched for effects on cranial skeleton development and pigment biosynthesis, reflecting the most divergent phenotypes observed between specialist species. Our findings reveal that even divergent niche specialists may exhibit convergent adaptation to higher trophic levels through shared genetic pathways. This counterintuitive result suggests that parallel evolution in gene expression can accompany divergent ecological speciation during adaptive radiation.\n\nImpact SummaryAdaptations that result in unique forms of ecological specialization are central to research in evolutionary biology, yet little is known about their molecular foundations. We combined transcriptome sequencing with whole-genome divergence scans to study the molecular evolution of two specialist Cyprinodon pupfish species - a scale-eater and a snail-eater - that rapidly diverged from a sympatric generalist ancestor within the last 10,000 years. While parallel evolution of gene expression driving convergent niche specialization seems common, we present, to our knowledge, the first example of significant parallel changes in expression coinciding with divergent niche specialization. 80% of genes that were differentially expressed between snail-eaters and generalists showed the same direction of expression in scale-eaters relative to generalists. Furthermore, parallel evolution in expression seem to be controlled by unique genetic variants in each specialist species. Genes showing parallel changes in expression were enriched for metabolic processes that may facilitate adaptation to a higher trophic level, while genes showing divergent expression likely shape the striking morphological differences between specialists. These findings contribute to a more nuanced understanding of convergent adaptations that arise during speciation, and highlight how species can evolve similar expression profiles adapted to divergent niches.

evolutionary biology↗

bioRxiv2018

Convergent regulatory evolution and the origin of flightlessness in palaeognathous birds

The relative roles of regulatory and protein evolution in the origin and loss of convergent phenotypic traits is a core question in evolutionary biology. Here we combine phylogenomic, epigenomic and developmental data to show that convergent evolution of regulatory regions, but not protein-coding genes, is associated with flightlessness in palaeognathous birds, a classic example of a convergent phenotype. Eleven new genomes, including a draft genome from an extinct moa, resolve palaeognath phylogeny and show that the incidence of independent, convergent accelerations among 284,000 conserved non-exonic elements is significantly more frequent in ratites than other bird lineages. Ratite-specific acceleration of conserved regions and measures of open chromatin across eight tissues in the developing chick identify candidate regulatory regions that may have modified or lost function in ratites. Enhancer activity assays conducted in the early developing chicken forelimb confirm that volant versions of a conserved element in the first intron of the TEAD1 gene display conserved enhancer activity, whereas an accelerated flightless version fails to drive reporter gene expression. Our results show that convergent molecular changes associated with loss of flight are largely regulatory in nature.

evolutionary biology↗

bioRxiv2017

Comparative transcriptomics reveals lineage specific evolution of cold response in Pooideae

BackgroundUnderstanding how complex traits evolve through adaptive changes in gene regulation remains a major challenge in evolutionary biology. Over the last ~50 million years, Earth has experienced climate cooling and ancestrally tropical plants have adapted to expanding temperate environments. The grass subfamily Pooideae dominates the grass flora of the temperate regions, but the role of cold-response gene regulation in the transitioning from tropical to temperate climate remains unexplored.\n\nResultsTo establish if molecular responses to cold are conserved throughout the phylogeny, we assembled the transcriptomes of five Pooideae species spanning early to later diverging lineages, and compared short- and long-term cold responsive genes using 8633 high confidence ortholog groups with resolved gene tree topologies. We found that a majority of cold responsive genes were specific to one or two lineages, an observation that we deem incompatible with a cold adapted Pooideae ancestor. However, all five species shared short-term cold response in a small set of general stress genes as well as the ability to down-regulate the photosynthetic machinery during cold temperatures.\n\nConclusionsOur observations indicate that the different Pooideae lineages have assembled cold response programs in parallel by taking advantage of a common potential for cold adaptation.

evolutionary biology↗

bioRxiv2014

An amino acid polymorphism in the Drosophila insulin receptor demonstrates pleiotropic and adaptive function in life history traits

Finding the specific nucleotides that underlie adaptive variation is a major goal in evolutionary biology, but polygenic traits pose a challenge because the complex genotype-phenotype relationship can obscure the effects of individual alleles. However, natural selection working in large wild populations can shift allele frequencies and indicate functional regions of the genome. Previously, we showed that the two most common alleles of a complex amino acid insertion-deletion polymorphism in the Drosophila insulin receptor show independent, parallel clines in frequency across the North American and Australian continents. Here, we report that the cline is stable over at least a five-year period and that the polymorphism also demonstrates temporal shifts in allele frequency concurrent with seasonal change. We tested the alleles for effects on levels of insulin signaling, fecundity, development time, body size, stress tolerance, and lifespan. We find that the alleles are associated with predictable differences in these traits, consistent with patterns of Drosophila life history variation across geography that likely reflect adaptation to the heterogeneous climatic environment. These results implicate insulin signaling as a major mediator of life history adaptation in Drosophila, and suggest that life history tradeoffs can be explained by extensive pleiotropy at a single locus.

Evolutionary Biology↗

bioRxiv2017

A Non-Classical Phase Diagram for Virus-Bacterial Co-Evolution Mediated by CRISPR

CRISPR is a newly discovered prokaryotic immune system. Bacteria and archaea with this system incorporate genetic material from invading viruses into their genomes, providing protection against future infection by similar viruses. The conditions for coexistence of prokaryots and viruses is an interesting problem in evolutionary biology. In this work, we show an intriguing phase diagram of the virus extinction probability, which is more complex than that of the classical predator-prey model. As the CRISPR incorporates genetic material, viruses are under pressure to evolve to escape the recognition by CRISPR. When bacteria have a small rate of deleting spacers, a new parameter region in which bacteria and viruses can coexist arises, and it leads to a more complex coexistence patten for bacteria and viruses. For example, when the virus mutation rate is low, the virus extinction probability changes non-montonically with the bacterial exposure rate. The virus and bacteria co-evolution not only alters the virus extinction probability, but also changes the bacterial population structure. Additionally, we show that recombination is a successful strategy for viruses to escape from CRISPR recognition when viruses have multiple proto-spacers, providing support for a recombination-mediated escape mechanism suggested experimentally. Finally, we suggest that the reentrant phase diagram, in which phages can progress through three phases of extinction and two phases of abundance at low spacer deletion rates as a function of exposure rate to bacteria, is an experimentally testable phenomenon.

evolutionary biology↗

bioRxiv2017

The demographic history and mutational load of African hunter-gatherers and farmers

The distribution of deleterious genetic variation across human populations is a key issue in evolutionary biology and medical genetics. However, the impact of different modes of subsistence on recent changes in population size, patterns of gene flow, and deleterious mutational load remains unclear. Here, we report high-coverage exome sequencing data from various populations of rainforest hunter-gatherers and farmers from central Africa. We find that the recent demographic histories of hunter-gatherers and farmers differed considerably, with population collapses for hunter-gatherers and expansions for farmers, accompanied by increased gene flow. We show that purifying selection against deleterious alleles is of similar efficiency across African populations, in contrast with Europeans where we detect weaker purifying selection. Furthermore, the per-individual mutation load of rainforest hunter-gatherers is similar to that of farmers, under both additive and recessive models. Our results indicate that differences in the cultural practices and demographic regimes of African populations have not resulted in large differences in mutational burden, and highlight the beneficial role of gene flow in reshaping the distribution of deleterious genetic variation across human populations.

evolutionary biology↗

bioRxiv2018

On the timing of bill length evolution in British great tits: A comment on Bosse et al. 2017.

Long-term field studies coupled with quantitative genomics offer a powerful means to understand the genetic bases underlying quantitative traits and their evolutionary changes. However, analyzing and interpreting the time scales at which adaptive evolution occurs is challenging. First, while evolution is predictable in the short term, with strikingly rapid phenotypic changes in data series, it remains unpredictable in the long term. Second, while the temporal dynamics of some loci with large effect on phenotypic variation and fitness have been characterized, this task can be complicated in cases of highly polygenic trait architecture implicating numerous small effect size loci, or when statistical tests are sensitive to the heterogeneity of some key characteristics of the genome, like recombination rate variations. After introducing these aforementioned challenges, we discuss a recent investigation of the genomic architecture and spatio-temporal variation in great tit bill length, which was related to the recent use of bird feeders. We discuss how this case study illustrates the importance of considering different temporal scales and evolutionary mechanisms both while analyzing trait temporal trends and when searching for and interpreting the signals of putative genomic footprints of selection. More generally this commentary discusses interesting challenges for unraveling the time scale at which adaptive traits evolve and their genomic bases.\n\nImpact summaryAn important goal in evolutionary biology is to understand how individual traits evolve, leading to fascinating variations in time and space. Long-term field studies have been crucial in trying to understand the timing, extent, and ecological determinants of such trait variation in wild populations. In this context, recent genomic tools can be used to look for the genetic bases underlying such trait variation and can provide clues on the nature and timing of their evolution. However, the analysis and the interpretation of the time scales at which evolution occurs remain challenging. First, analyzing long-term data series can be tricky; short-term changes are highly predictable whereas long-term evolution is much less predictable. A second difficult task is to study the architecture of complex quantitative traits and to decipher the timing and roles of the several genomic mechanisms involved in their evolution. This commentary introduces these challenges and discusses a recent investigation of the nature and timing of ecological and genomic factors responsible for variation in great tit bill length. Overall, we raise cautionary warnings regarding several conceptual and technical features and limitations when coupling analyses of long-term and genomic data to study trait evolution in wild populations.

evolutionary biology↗