Ecological speciation promoted by divergent regulation of functional genes within African cichlid fishes

Rapid ecological speciation along depth gradients has taken place independently and repeatedly in freshwater fishes. While the extent of genomic divergence between ecomorphs is often well understood, the molecular mechanisms facilitating such rapid diversification are typically unclear. In Lake Masoko, an East African crater lake, the cichlid Astatotilapia calliptera has diverged into shallow littoral and deep benthic ecomorphs with strikingly different jaw structures within the last 1,000 years. Using genome-wide transcriptome data from jaw tissue, we explore two major regulatory transcriptional mechanisms, expression and splicing QTL variants and examine their contribution to differential gene expression underpinning functional phenotypes. We identified 7,550 genes with significant differential expression between ecomorphs, of which 4.2% were regulated by cis-regulatory expression QTLs, and 6.4% were regulated by cis-regulatory splicing QTLs. There were also strong signals of divergent selection of differentially expressed genes that showed divergent regulation from expression, splicing or both QTL variants, including genes associated with major jaw plasticity and adaptation networks, adaptive immune system response, and oxidoreductase processes. These results suggest that transcriptome plasticity and modification have important roles during early-stage ecological speciation and demonstrate the role of regulatory-variants as important targets of selection driving ecologically-relevant divergence in gene expression that is associated with adaptive diversification.

Lineage-Specific Genes and Family Expansions in Dictyostelid Genomes Display Expression Bias and Evolutionary Diversification during Development

Gene duplications generate new genes that can contribute to expression changes and the evolution of new functions. Genomes often consist of gene families that undergo expansions, some of which occur in specific lineages that reflect recent adaptive diversification. In this study, lineage-specific genes and gene family expansions were studied across five dictyostelid species to determine when and how they are expressed during multicellular development. Lineage-specific genes were found to be enriched among genes with biased expression (predominant expression in one developmental stage) in each species and at most developmental time points, suggesting independent functional innovations of new genes throughout the phylogeny. Biased duplicate genes had greater expression divergence than their orthologs and paralogs, consistent with subfunctionalization or neofunctionalization. Lineage-specific expansions in particular had biased genes with both molecular signals of positive selection and high expression, suggesting adaptive genetic and transcriptional diversification following duplication. Our results present insights into the potential contributions of lineage-specific genes and families in generating species-specific phenotypes during multicellular development in dictyostelids.

Mapping epigenetic divergence in the massive radiation of Lake Malawi cichlid fishes

Epigenetic variation modulates gene expression and can be heritable. However, knowledge of the contribution of epigenetic divergence to adaptive diversification in nature remains limited. The massive evolutionary radiation of Lake Malawi cichlid fishes displaying extensive phenotypic diversity despite extremely low sequence divergence is an excellent system to study the epigenomic contribution to adaptation. Here, we present a comparative genome-wide methylome and transcriptome study, focussing on liver and muscle tissues in phenotypically divergent cichlid species. In both tissues we find substantial methylome divergence among species. Differentially methylated regions (DMR), enriched in evolutionary young transposons, are associated with transcription changes of ecologically-relevant genes related to energy expenditure and lipid metabolism, pointing to a link between dietary ecology and methylome divergence. Unexpectedly, half of all species-specific DMRs are shared across tissues and are enriched in developmental genes, likely reflecting distinct epigenetic developmental programmes. Our study reveals substantial methylome divergence in closely-related cichlid fishes and represents a resource to study the role of epigenetics in species diversification.

Niche shifts after island colonization spurred adaptive diversification and speciation in a cosmopolitan bird clade

Islands have long been recognized as key contributors to biodiversity because they facilitate geographic isolation and ecological divergence from mainland ancestors. However, island colonization has traditionally been considered an evolutionary dead-end process, and its consequences for continental biodiversity remain understudied. Here, we use the evolutionary radiation of Columbiformes (i.e. pigeons and doves) to examine if ecological niche shifts on islands shaped biological diversification and community composition on continents. We show that the colonization of islands by continental, terrestrial-foraging lineages led to the exploitation of a new ecological niche (i.e. arboreal foraging). This transition towards arboreal foraging was associated with evolutionary adaptation towards a new morphological optimum. In addition, arboreal-foraging lineages of islands experienced an increase in speciation rates, which was associated with successful range expansions to other islands as well as back colonization of continents. Our results provide empirical evidence that diversification on continents can only be fully understood when studying the diversification processes that took place on islands, challenging the view of islands as mere sinks of evolutionary diversity.

Signatures of adaptive evolution in platyrrhine primate genomes

The family Cebidae (capuchin and squirrel monkeys) form a remarkable platyrrhine clade exhibiting among the largest primate encephalisation quotients. Each cebid lineage is characterised by notable lineage-specific traits, with capuchins showing striking similarities to Hominidae including high sensorimotor intelligence with tool use, advanced cognitive abilities, and behavioural flexibility. Here, we take a comparative genomics approach, analysing five cebid branches including successive lineages, to infer a stepwise timeline for cebid adaptive evolution. We uncover candidate targets of selection across various periods of cebid evolution that may underlie the emergence of lineage-specific traits. Our analyses highlight shifting and sustained selective pressures on genes related to brain development, longevity, reproduction, and morphology, including evidence for cumulative and diversifying neurobiological adaptations over cebid evolutionary history. In addition to generating a new, high-quality reference genome assembly for robust capuchins, our results lend to a better understanding of the adaptive diversification of this distinctive primate clade.

Interspecific Niche Competition Increases Morphological Diversity in Multi-Species Microbial Communities

Intraspecific competition for limited niches has been recognized as a driving force for adaptive radiation, but results for the role of interspecific competition have been mixed. Here, we report the adaptive diversification of the model bacteria Pseudomonas fluorescens in the presence of different numbers and combinations of four competing bacterial species. Increasing the diversity of competitive community increased the morphological diversity of focal species, which is caused by impeding the domination of a single morphotype. Specifically, this pattern was driven by more diverse communities being more likely to contain key species that occupy the same niche as otherwise competitively superior morphotype, and thus preventing competitive exclusion within the focal species. Our results suggest that sympatric adaptive radiation is driven by the presence or absence of niche-specific competitors.

Topology and habitat assortativity drive neutral and adaptive diversification in spatial graphs

Biodiversity results from differentiation mechanisms developing within biological populations. Such mechanisms are influenced by the properties of the landscape over which individuals interact, disperse and evolve. Notably, landscape connectivity and habitat heterogeneity constrain the movement and survival of individuals, thereby promoting differentiation through drift and local adaptation. Nevertheless, the complexity of landscape features can blur our understanding of how they drive differentiation. Here, we formulate a stochastic, eco-evolutionary model where individuals are structured over a graph that captures complex connectivity patterns and accounts for habitat heterogeneity. Individuals possess neutral and adaptive traits, whose divergence results in differentiation at the population level. The modelling framework enables an analytical underpinning of emerging macroscopic properties, which we complement with numerical simulations to investigate how the graph topology and the spatial habitat distribution affect differentiation. We show that in the absence of selection, graphs with high characteristic length and high heterogeneity in degree promote neutral differentiation. Habitat assortativity, a metric that captures habitat spatial auto-correlation in graphs, additionally drives differentiation patterns under habitat-dependent selection. While assortativity systematically amplifies adaptive differentiation, it can foster or depress neutral differentiation depending on the migration regime. By formalising the eco-evolutionary and spatial dynamics of biological populations in complex landscapes, our study establishes the link between landscape features and the emergence of diversification, contributing to a fundamental understanding of the origin of biodiversity gradients.

Asynchronous rates of lineage, phenotype, and niche diversification in a continental-scale adaptive radiation

Rapidly diversifying clades are central to the study of diversification dynamics. This central importance is perhaps most apparent when rapid evolution occurs across several axes of diversification (e.g., lineage, phenotype, and niche); such clades facilitate investigations into the interplay between adaptive and non-adaptive diversification mechanisms. Yet, empirical evidence from rapidly evolving clades remains unclear about the relationships, if any, across diversification axes. This is especially apparent regarding the timing of diversification rate shifts. We address this knowledge gap through comparisons of the rate and timing of lineage, phenotypic, and niche diversification in Penstemon, a rapidly-evolving angiosperm genus. We find that diversification rate shifts in Penstemon are asynchronous; while we identify a burst and subsequent slowdown in lineage diversification rate ~2.0-2.5 MYA, shifts in phenotypic and niche diversification rates either lagged behind temporally or did not occur at all. We posit that this asynchronicity in diversification rate shifts is the result of initial niche-neutral diversification followed by adaptive, density-dependent processes. Our findings contribute to a growing body of evidence that asynchronous shifts in diversification rates may be common and question the applicability of expectations for diversification dynamics across disparate empirical systems.

Adaptive diversification in the cellular circadian behavior of Arabidopsis leaf- and root-derived cells

The plant circadian system is based on self-sustained cellular oscillations and is utilized to adapt to daily and seasonal environmental changes. The cellular circadian clocks in the above- and belowground plant organs are subjected to diverse local environments. Individual cellular clocks are affected by other cells/tissues in plants, and the intrinsic properties of cellular clocks remain to be elucidated. In this study, we showed the circadian properties of leaf- and root-derived cells of a CCA1::LUC Arabidopsis transgenic plant and demonstrated that the cells in total isolation from other cells harbor a genuine circadian clock. Quantitative and statistical analyses for individual cellular bioluminescence rhythms revealed a difference in amplitude and precision of light/dark entrainment between the two cell-types, suggesting that leaf-derived cells have a clock with a stronger persistence against fluctuating environments. Circadian systems in the leaves and roots are diversified to adapt to their local environments at the cellular level.