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Climatic niche change of fish is faster at high latitude and in marine environments

Change in species climatic niches is a key mechanism influencing species distribution patterns. The question of which factors impact niche change remains a highly debated topic in evolutionary biology. Previous studies have proposed that rates of climatic niche change might be correlated with climatic oscillations at high latitude or adaptation to new environmental conditions. Yet, very few studies have asked if those factors are also predominant in aquatic environments. Here, we reconstruct the climatic niche changes of fish species on a new phylogeny encompassing 12,616 species. We first confirm that the rate of niche change is faster at high latitude and show that this association is steeper for freshwater than for marine species. We also show that freshwater species have slower rates of niche change than marine species. These results may be explained by the fact that freshwater species have larger climatic niche breadth and thermal safety margin than marine species at high latitude. Overall, our study sheds a new light on the environmental conditions and species features impacting rates of climatic niche change in aquatic habitats.

evolutionary biology↗

Emergence of Genetic Sex Determination in an Environmentally Sex-Determined Animal

The evolution of genetic sex determination (GSD) from environmental sex determination (ESD) remains a fundamental issue in evolutionary biology. However, the mechanisms driving such a transition, particularly in its earliest stages, are largely unknown. Here, we report on a genetic variant in the ESD species, Daphnia pulex, in which structural variations and selection on chromosome have suppressed recombination. This suppression has facilitated the accumulation of antagonistic features of the two chromosome- haplotypes, resulting in heterozygosity and differentiation of the sex-determining gene Dfh on two haplotypes. Consequently, this process has driven the emergence of a mixed-mating system, in which sex determination is jointly regulated by genetic and environmental factors. Additionally, we detected ongoing divergence in chromosomal structure between the two haplotypes at the population level. These findings suggest that processes analogous to early sex-chromosome evolution are occurring in this ESD species, offering novel insights into the molecular mechanisms underlying the emergence of GSD.

evolutionary biology↗

An ancient anthozoan protein reveals an alternative evolutionary path of antiviral signaling

How antiviral immunity first arose in animals is a central question in evolutionary biology. Using the sea anemone Nematostella vectensis, we identify CARDIB, a previously uncharacterized gene located next to RLRb, a cnidarian homolog of the vertebrate RIG-I-like receptor family. This conserved genomic linkage across Anthozoa reveals an ancient coupling between immune sensing and regulation. Despite sequence similarity to vertebrate MAVS, CARDIB performs an opposing function: it represses immune genes under basal conditions yet is essential for activation upon viral challenge. CARDIB binds RLRb via a single CARD domain, forming a repressive complex. Loss of either gene abolishes antiviral transcription, disrupts apoptosis, and elevates viral load under lab conditions. Both genes as well as the RLRb paralog, RLRa, are essential for antiviral defense under native conditions. Phylogeny places the cnidarian CARDs distinctly from the vertebrate RLR-MAVS families, revealing an ancient antiviral system regulating antiviral response through CARD-based signaling.

evolutionary biology↗

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↗

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↗

Nano-computed tomography reveals repeated phenotypic divergence in parasites to escape host defense

Understanding how selective pressures drive morphological change is a central question in evolutionary biology. Feather lice have repeatedly diversified into convergent ecomorphs, based on how they escape from host defenses in different microhabitats. Here, we used nano-computed tomography scan data of 89 specimens of feather lice, belonging to four ecomorph groups to quantify variation of functional traits, including mandibular muscle volume, limb length, and three-dimensional head shape data in these tiny insects. The results suggest that the shape of the head, the proportional volume of the chewing muscles, and the length of the leg segments in feather lice are all strongly associated with specific host-habitats. Further, species that co-occur on hosts have increased rates of morphological evolution, suggesting competition for host space is one of the drivers of morphology. This supports previous work indicating that the phenotypic diversity of feather lice is the result of repeated convergence resulting from resource partitioning, microhabitat specialization, and selection pressures imposed by host defense.

evolutionary biology↗

Allopatric speciation in cattails: Genomic landscapes of divergence across Typha spp. suggest balancing selection, introgressions, and the absence of adaptive divergence

Understanding how speciation unfolds is a central goal of evolutionary biology. Historically, global climatic fluctuations have triggered allopatric diversification. Using genome-wide data, we reconstructed the phylogenetic relationships and demographic histories of five Typha species, a plant genus foundational to freshwater ecosystems, with widespread, partially sympatric ranges and at least one widespread, regionally invasive hybrid zone (Typha x glauca). Molecular clock and demographic analyses indicate that the species in this study diverged in the absence of gene flow, during periods roughly contemporaneous with population bottlenecks and expansions in Typha--likely triggered by geoclimatic events--and that this divergence was followed by secondary contact in more recent times. Genomic scans showed no evidence of selection with gene flow driving species differentiation, suggesting a minor role for sympatric ecological speciation underlying divergence. These observations are consistent with expectations for drift-driven allopatric speciation. Allopatric speciation in T. latifolia and T. angustifolia, their low genetic differentiation, and the scarcity of ecological divergence in building their reproductive isolation could explain these species ability to hybridise.

evolutionary biology↗

A chromosomal inversion drives evolution of multiple adaptive traits in deer mice

A long-standing question in evolutionary biology is how differences in multiple traits can evolve quickly and be maintained together during local adaptation. Using forest and prairie ecotypes in deer mice, which differ in both tail length and coat color, we discovered a 41 Mb chromosomal inversion that is strongly linked to variation in both traits. The inversion maintains highly divergent loci in strong linkage disequilibrium and likely originated ~170 kya, long before the forest-prairie divergence ~10 kya. Consistent with a role in local adaptation, inversion frequency is associated with phenotype and habitat across both a local transect and the species range. Still, although eastern and western forest subspecies share similar phenotypes, the inversion is absent in eastern North America. This work highlights the significance of inversion polymorphisms for the establishment and maintenance of multiple locally adaptive traits in mammals, and demonstrates that, even within a species, parallel phenotypes may evolve through nonparallel genetic mechanisms.

evolutionary biology↗

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↗

LEA 3: Factor models in population genetics and ecological genomics with R

A major objective of evolutionary biology is to understand the processes by which organisms have adapted to various environments, and to predict the response of organisms to new or future conditions. The availability of large genomic and environmental data sets provides an opportunity to address those questions, and the R package LEA has been introduced to facilitate population and ecological genomic analyses in this context. By using latent factor models, the program computes ancestry coefficients from population genetic data, and performs genotype-environment association analyses with correction for unobserved confounding variables. In this study, we present new functionalities of LEA, which include imputation of missing genotypes, fast algorithms for latent factor mixed models using multivariate predictors for genotype-environment association studies, population differentiation tests for admixed or continuous populations, and estimation of genetic offset based on climate models. The new functionalities are implemented in version 3.0 and higher releases of the package. Using simulated and real data sets, our study provides evaluations and examples of applications, outlining important practical considerations when analyzing ecological genomic data in R.

evolutionary biology↗

Facultative Cheating and Hybrid Vigor Resolves Cooperator-Cheater Conflict in a Yeast Public Goods System.

The persistence of cooperation in the face of cheating is a central paradox in evolutionary biology. Microbial public goods systems employ diverse solutions to this dilemma, yet most studies assume fixed strategies wherein genotypes function strictly as cooperators or cheaters. Here, using the GAL/MEL regulon of Saccharomyces cerevisiae, we uncover a dynamic resolution to this conflict through facultative strategy switching. When haploid cheater-cooperator strains were co-evolved in melibiose, we observed the repeated emergence of same-mating-type diploid hybrids. These hybrids arise early in evolution and ultimately spread in the population. The hybrids exploit the public good produced by cooperator strains when present, acting as facultative cheaters. However, following cooperator extinction, hybrids switch to a cooperative phenotype. This dynamic role transition enables the hybrid to persist across shifting ecological contexts. Our findings reveal a novel, context-dependent mechanism of cooperation maintenance, whereby facultative cheating and genotype plasticity resolve the tension between individual fitness and collective benefit. This work expands the conceptual framework of social evolution by demonstrating that phenotypic flexibility, facilitated through hybridization, can stabilize cooperation even in fully exploitable public goods systems.

evolutionary biology↗

Epigenetic variations are landmarks of freshwater adaptation in threespine sticklebacks

For evolutionary biology, the phenotypic consequences of epigenetic variations and their potential contribution to adaptation and diversification are pressing issues. Marine and freshwater sticklebacks represent an ideal model for studying both genetic and epigenetic components of phenotypic plasticity that allow fish to inhabit water with different salinity. Here, we applied single-cell genomics (scRNA-seq and scATAC-seq) and whole-genome bisulfite sequencing to characterize intercellular variability in transcription, the abundance of open chromatin regions, and CpG methylation level in gills of marine and freshwater stickleback morphs. We found little difference in overall transcriptional variance between the morphs but observed significant changes in chromatin openness variance. In addition, genomic divergence islands (DIs) coincided with regions of increased methylation entropy in freshwater fish. Moreover, analysis of transcription factor binding sites within DIs revealed that [C]TCF motifs around marker SNPs were significantly enriched within the region. Altogether, our data show that increased epigenetic variance accompanies the adaptation of marine sticklebacks to freshwater.

evolutionary biology↗

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↗

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↗

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↗

Predicting fitness related traits using gene expression and machine learning

Evolution by natural selection occurs at its most basic through the change in frequencies of alleles; connecting those genomic targets to phenotypic selection is an important goal for evolutionary biology in the genomics era. The relative abundance of gene products expressed in a tissue can be considered a phenotype intermediate to the genes and genomic regulatory elements themselves, and more traditionally measured macroscopic phenotypic traits such as flowering time, size, or growth. The high-dimensionality, low sample size nature of transcriptomic sequence data is a double-edged sword, however, as it provides abundant information but makes traditional statistics difficult. Machine learning has many features which handle high-dimensional data well and is thus useful in genetic sequence applications. Here we examined the association of fitness-components with gene expression data in Ipomoea hederacea (Ivyleaf Morning Glory) grown under field conditions. We combine the results of two different machine learning approaches and find evidence that expression of photosynthesis-related genes is likely under selection. We also find that genes related to stress and light response were overall important in predicting fitness. With this study we demonstrate the utility of machine learning models for smaller samples, and their potential application for understanding natural selection.

evolutionary biology↗

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↗

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↗