Patterson's D, also known as the ABBA‐BABA statistic, and related statistics such as the f4‐ratio, are commonly used to assess evidence of gene flow between populations or closely related species. ...Currently available implementations often require custom file formats, implement only small subsets of the available statistics, and are impractical to evaluate all gene flow hypotheses across data sets with many populations or species due to computational inefficiencies. Here, we present a new software package Dsuite, an efficient implementation allowing genome scale calculations of the D and f4‐ratio statistics across all combinations of tens or hundreds of populations or species directly from a variant call format (VCF) file. Our program also implements statistics suited for application to genomic windows, providing evidence of whether introgression is confined to specific loci, and it can also aid in interpretation of a system of f4‐ratio results with the use of the “f‐branch” method. Dsuite is available at https://github.com/millanek/Dsuite, is straightforward to use, substantially more computationally efficient than comparable programs, and provides a convenient suite of tools and statistics, including some not previously available in any software package. Thus, Dsuite facilitates the assessment of evidence for gene flow, especially across larger genomic data sets.
Powerful approaches to inferring recent or current population structure based on nearest neighbor haplotype "coancestry" have so far been inaccessible to users without high quality genome-wide ...haplotype data. With a boom in nonmodel organism genomics, there is a pressing need to bring these methods to communities without access to such data. Here, we present RADpainter, a new program designed to infer the coancestry matrix from restriction-site-associated DNA sequencing (RADseq) data. We combine this program together with a previously published MCMC clustering algorithm into fineRADstructure-a complete, easy to use, and fast population inference package for RADseq data (https://github.com/millanek/fineRADstructure; last accessed February 24, 2018). Finally, with two example data sets, we illustrate its use, benefits, and robustness to missing RAD alleles in double digest RAD sequencing.
The hundreds of cichlid fish species in Lake Malawi constitute the most extensive recent vertebrate adaptive radiation. Here we characterize its genomic diversity by sequencing 134 individuals ...covering 73 species across all major lineages. The average sequence divergence between species pairs is only 0.1-0.25%. These divergence values overlap diversity within species, with 82% of heterozygosity shared between species. Phylogenetic analyses suggest that diversification initially proceeded by serial branching from a generalist Astatotilapia-like ancestor. However, no single species tree adequately represents all species relationships, with evidence for substantial gene flow at multiple times. Common signatures of selection on visual and oxygen transport genes shared by distantly related deep-water species point to both adaptive introgression and independent selection. These findings enhance our understanding of genomic processes underlying rapid species diversification, and provide a platform for future genetic analysis of the Malawi radiation.
Adaptive radiation is the likely source of much of the ecological and morphological diversity of life
. How adaptive radiations proceed and what determines their extent remains unclear in most cases
.... Here we report the in-depth examination of the spectacular adaptive radiation of cichlid fishes in Lake Tanganyika. On the basis of whole-genome phylogenetic analyses, multivariate morphological measurements of three ecologically relevant trait complexes (body shape, upper oral jaw morphology and lower pharyngeal jaw shape), scoring of pigmentation patterns and approximations of the ecology of nearly all of the approximately 240 cichlid species endemic to Lake Tanganyika, we show that the radiation occurred within the confines of the lake and that morphological diversification proceeded in consecutive trait-specific pulses of rapid morphospace expansion. We provide empirical support for two theoretical predictions of how adaptive radiations proceed, the 'early-burst' scenario
(for body shape) and the stages model
(for all traits investigated). Through the analysis of two genomes per species and by taking advantage of the uneven distribution of species in subclades of the radiation, we further show that species richness scales positively with per-individual heterozygosity, but is not correlated with transposable element content, number of gene duplications or genome-wide levels of selection in coding sequences.
The genomic causes and effects of divergent ecological selection during speciation are still poorly understood. Here we report the discovery and detailed characterization of early-stage adaptive ...divergence of two cichlid fish ecomorphs in a small (700 meters in diameter) isolated crater lake in Tanzania. The ecomorphs differ in depth preference, male breeding color, body shape, diet, and trophic morphology. With whole-genome sequences of 146 fish, we identified 98 clearly demarcated genomic "islands" of high differentiation and demonstrated the association of genotypes across these islands with divergent mate preferences. The islands contain candidate adaptive genes enriched for functions in sensory perception (including rhodopsin and other twilight-vision–associated genes), hormone signaling, and morphogenesis. Our study suggests mechanisms and genomic regions that may play a role in the closely related mega-radiation of Lake Malawi.
Abstract
The adaptive radiation of cichlid fishes in East African Lake Malawi encompasses over 500 species that are believed to have evolved within the last 800,000 years from a common founder ...population. It has been proposed that hybridization between ancestral lineages can provide the genetic raw material to fuel such exceptionally high diversification rates, and evidence for this has recently been presented for the Lake Victoria region cichlid superflock. Here, we report that Lake Malawi cichlid genomes also show evidence of hybridization between two lineages that split 3–4 Ma, today represented by Lake Victoria cichlids and the riverine Astatotilapia sp. “ruaha blue.” The two ancestries in Malawi cichlid genomes are present in large blocks of several kilobases, but there is little variation in this pattern between Malawi cichlid species, suggesting that the large-scale mosaic structure of the genomes was largely established prior to the radiation. Nevertheless, tens of thousands of polymorphic variants apparently derived from the hybridization are interspersed in the genomes. These loci show a striking excess of differentiation across ecological subgroups in the Lake Malawi cichlid assemblage, and parental alleles sort differentially into benthic and pelagic Malawi cichlid lineages, consistent with strong differential selection on these loci during species divergence. Furthermore, these loci are enriched for genes involved in immune response and vision, including opsin genes previously identified as important for speciation. Our results reinforce the role of ancestral hybridization in explosive diversification by demonstrating its significance in one of the largest recent vertebrate adaptive radiations.
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.
Evolutionary radiations are responsible for much of the variation in biodiversity across taxa. Cichlid fishes are well known for spectacular evolutionary radiations, as they have repeatedly evolved ...into large and phenotypically diverse arrays of species. Cichlid genomes carry signatures of past events and, at the same time, are the substrate for ongoing evolution. We survey genome-wide data and the available literature covering 438 cichlid populations (412 species) across multiple radiations to synthesize information about patterns and sharing of genetic variation. Nucleotide diversity within species is low in cichlids, with 92% of surveyed populations having less diversity than the median value found in other vertebrates. Divergence within radiations is also low, and a large proportion of variation is shared among species due to incomplete lineage sorting and widespread hybridization. Population genetics therefore provides a suitable conceptual framework for evolutionary genomic studies of cichlid radiations. We focus in detail on the roles of hybridization in shaping the patterns of genetic variation and in promoting cichlid diversification.
Lake Malawi cichlid fishes exhibit extensive divergence in form and function built from a relatively small number of genetic changes. We compared the genomes of rock- and sand-dwelling species and ...asked which genetic variants differed among the groups. We found that 96% of differentiated variants reside in non-coding sequence but these non-coding diverged variants are evolutionarily conserved. Genome regions near differentiated variants are enriched for craniofacial, neural and behavioral categories. Following leads from genome sequence, we used rock- vs. sand-species and their hybrids to (i) delineate the push-pull roles of BMP signaling and irx1b in the specification of forebrain territories during gastrulation and (ii) reveal striking context-dependent brain gene expression during adult social behavior. Our results demonstrate how divergent genome sequences can predict differences in key evolutionary traits. We highlight the promise of evolutionary reverse genetics-the inference of phenotypic divergence from unbiased genome sequencing and then empirical validation in natural populations.
PDF
