Population genetic and phylogenetic insights into the adaptive radiation of Antarctic notothenioid fishes

Adaptive radiation is the evolution of ecological and phenotypic diversity within a rapidly multiplying lineage, a phenomenon that is considered responsible for a great part of Earthʼs biodiversity. It occurs as a response to ecological opportunity in the form of competitor-free habitat, extinction of antagonists, or the emergence of a key innovation. One of the most spectacular adaptive radiations in the marine realm is the diversification of notothenioid fishes in the freezing waters of Antarctica. This radiation has led to a unique dominance of the Antarctic marine habitat by notothenioids, and is often assumed to result from the key innovation of freeze resistance. Antifreeze glycoproteins are present in blood and tissue of Antarctic notothenioids and enable them to survive in their sub-zero environment. Notothenioids are further characterized by prolonged pelagic larval stages, that have been suggested to contribute to high levels of inter-population gene flow with oceanic currents, which seems to contradict the high speciation rates observed in the notothenioid adaptive radiation. This doctoral work uses molecular tools to investigate the character of gene flow in notothenioids as well as the origin of their diversification. It is demonstrated that larval dispersal is a common agent of long-distance gene flow in many notothenioid species. The key innovation hypothesis is corroborated by an extensive molecular dating of the divergence events of notothenioids and related acanthomorph fishes. New tools for the analysis of microsatellite markers and for Bayesian divergence date estimation are developed

TANDEM: integrating automated allele binning into genetics and genomics workflows

Summary: Computer programs for the statistical analysis of microsatellite data use allele length variation to infer, e.g. population genetic parameters, to detect quantitative trait loci or selective sweeps. However, observed allele lengths are usually inaccurate and may deviate from the expected periodicity of repeats. The common practice of rounding to the nearest whole number frequently results in miscalls and underestimations of allelic richness. Manual sorting of allele lengths into discrete classes, a process called binning, is tedious and error-prone. Here, we present a new program for the automated binning of microsatellite allele lengths to overcome these problems and to facilitate high-throughput allele binning. Availability: www.evolution.unibas.ch/salzburger/software.htm Contact: [email protected] Supplementary information: Supplementary data are available at Bioinformatics onlin

Disentangling Incomplete Lineage Sorting and Introgression to Refine Species-Tree Estimates for Lake Tanganyika Cichlid Fishes

Adaptive radiation is thought to be responsible for the evolution of a great portion of the past and present diversity of life. Instances of adaptive radiation, characterized by the rapid emergence of an array of species as a consequence to their adaptation to distinct ecological niches, are important study systems in evolutionary biology. However, because of the rapid lineage formation in these groups, and occasional gene flow between the participating species, it is often difficult to reconstruct the phylogenetic history of species that underwent an adaptive radiation. In this study, we present a novel approach for species-tree estimation in rapidly diversifying lineages, where introgression is known to occur, and apply it to a multimarker data set containing up to 16 specimens per species for a set of 45 species of East African cichlid fishes (522 individuals in total), with a main focus on the cichlid species flock of Lake Tanganyika. We first identified, using age distributions of most recent common ancestors in individual gene trees, those lineages in our data set that show strong signatures of past introgression. This led us to formulate three hypotheses of introgression between different lineages of Tanganyika cichlids: the ancestor of Boulengerochromini (or of Boulengerochromini and Bathybatini) received genomic material from the derived H-lineage; the common ancestor of Cyprichromini and Perissodini experienced, in turn, introgression from Boulengerochromini and/or Bathybatini; and the Lake Tanganyika Haplochromini and closely related riverine lineages received genetic material from Cyphotilapiini. We then applied the multispecies coalescent model to estimate the species tree of Lake Tanganyika cichlids, but excluded the lineages involved in these introgression events, as the multispecies coalescent model does not incorporate introgression. This resulted in a robust species tree, in which the Lamprologini were placed as sister lineage to the H-lineage (including the Eretmodini), and we identify a series of rapid splitting events at the base of the H-lineage. Divergence ages estimated with the multispecies coalescent model were substantially younger than age estimates based on concatenation, and agree with the geological history of the Great Lakes of East Africa. Finally, we formally tested the three hypotheses of introgression using a likelihood framework, and find strong support for introgression between some of the cichlid tribes of Lake Tanganyika. [Adaptive radiation; Cichlidae; introgression; Lake Tanganyika; species network.]

Dynamics of sex chromosome evolution in a rapid radiation of cichlid fishes

[Figure: see text]

Estimating uncertainty in divergence times among three-spined stickleback clades using the multispecies coalescent

Incomplete lineage sorting (ILS) can lead to biased divergence time estimates. To explore if and how ILS has influenced the results of a recent study of worldwide phylogeny of three-spined sticklebacks (Gasterosteus aculeatus), we estimated divergence times among major clades by applying both a concatenation approach and the multispecies coalescent (MSC) model to single-nucleotide polymorphisms. To further test the influence of different calibration strategies, we applied different calibrations to the root and to younger nodes in addition to the ones used in the previous study. Both the updated calibrations and the application of the MSC model influenced divergence time estimates, sometimes significantly. The new divergence time estimates were more ancient than in the previous study for older nodes, whereas the estimates of younger nodes were not strongly affected by the re-analyses. However, given the applied MSC method employs a simple substitution model and cannot account for changes in population size, we suggest that different analytical approaches and calibration strategies should be used in order to explore uncertainty in divergence time estimates. This study provides a valuable reference timeline for the ages of worldwide three-spined stickleback populations and emphasizes the need to embrace, rather than obscure, uncertainties around divergence time estimates.Peer reviewe

Bayesian Phylogenetic Estimation of Clade Ages Supports Trans-Atlantic Dispersal of Cichlid Fishes

Divergence-time estimation based on molecular phylogenies and the fossil record has provided insights into fundamental questions of evolutionary biology. In Bayesian node dating, phylogenies are commonly time calibrated through the specification of calibration densities on nodes representing clades with known fossil occurrences. Unfortunately, the optimal shape of these calibration densities is usually unknown and they are therefore often chosen arbitrarily, which directly impacts the reliability of the resulting age estimates. As possible solutions to this problem, two nonexclusive alternative approaches have recently been developed, the "fossilized birth-death" (FBD) model and "total-evidence dating." While these approaches have been shown to perform well under certain conditions, they require including all (or a random subset) of the fossils of each clade in the analysis, rather than just relying on the oldest fossils of clades. In addition, both approaches assume that fossil records of different clades in the phylogeny are all the product of the same underlying fossil sampling rate, even though this rate has been shown to differ strongly between higher level taxa. We here develop a flexible new approach to Bayesian age estimation that combines advantages of node dating and the FBD model. In our new approach, calibration densities are defined on the basis of first fossil occurrences and sampling rate estimates that can be specified separately for all clades. We verify our approach with a large number of simulated data sets, and compare its performance to that of the FBD model. We find that our approach produces reliable age estimates that are robust to model violation, on par with the FBD model. By applying our approach to a large data set including sequence data from over 1000 species of teleost fishes as well as 147 carefully selected fossil constraints, we recover a timeline of teleost diversification that is incompatible with previously assumed vicariant divergences of freshwater fishes. Our results instead provide strong evidence for transoceanic dispersal of cichlids and other groups of teleost fishes. [Bayesian inference; calibration density; Cichlidae; fossil record; marine dispersal; phylogeny; relaxed molecular clock]

A High-Quality Assembly of the Nine-Spined Stickleback (Pungitius pungitius) Genome

The Gasterosteidae fish family hosts several species that are important models for eco-evolutionary, genetic, and genomic research. In particular, a wealth of genetic and genomic data has been generated for the three-spined stickleback (Gasterosteus aculeatus), the "ecology's supermodel," whereas the genomic resources for the nine-spined stickleback (Pungitius pungitius) have remained relatively scarce. Here, we report a high-quality chromosome-level genome assembly of P. pungitius consisting of 5,303 contigs (N50 = 1.2Mbp) with a total size of 521 Mbp. These contigs were mapped to 21 linkage groups using a high-density linkage map, yielding a final assembly with 98.5% BUSCO completeness. A total of 25,062 protein-coding genes were annotated, and about 23% of the assembly was found to consist of repetitive elements. A comprehensive analysis of repetitive elements uncovered centromere-specific tandem repeats and provided insights into the evolution of retrotransposons. A multigene phylogenetic analysis inferred a divergence time of about 26 million years ago (Ma) between nine- and three-spined sticklebacks, which is far older than the commonly assumed estimate of 13 Ma. Compared with the three-spined stickleback, we identified an additional duplication of several genes in the hemoglobin cluster. Sequencing data from populations adapted to different environments indicated potential copy number variations in hemoglobin genes. Furthermore, genome-wide synteny comparisons between three- and nine-spined sticklebacks identified chromosomal rearrangements underlying the karyotypic differences between the two species. The high-quality chromosome-scale assembly of the nine-spined stickleback genome obtained with long-read sequencing technology provides a crucial resource for comparative and population genomic investigations of stickleback fishes and teleosts.Peer reviewe

Drivers and dynamics of a massive adaptive radiation in cichlid fishes

Adaptive radiation is the likely source of much of the ecological and morphological diversity of life; 1-4; . How adaptive radiations proceed and what determines their extent remains unclear in most cases; 1,4; . 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; 1,5; (for body shape) and the stages model; 1,6,7; (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

Genomic stability through time despite decades of exploitation in cod on both sides of the Atlantic

The mode and extent of rapid evolution and genomic change in response to human harvesting are key conservation issues. Although experiments and models have shown a high potential for both genetic and phenotypic change in response to fishing, empirical examples of genetic responses in wild populations are rare. Here, we compare whole-genome sequence data of Atlantic cod (Gadus morhua) that were collected before (early 20th century) and after (early 21st century) periods of intensive exploitation and rapid decline in the age of maturation from two geographically distinct populations in Newfoundland, Canada, and the northeast Arctic, Norway. Our temporal, genome-wide analyses of 346,290 loci show no substantial loss of genetic diversity and high effective population sizes. Moreover, we do not find distinct signals of strong selective sweeps anywhere in the genome, although we cannot rule out the possibility of highly polygenic evolution. Our observations suggest that phenotypic change in these populations is not constrained by irreversible loss of genomic variation and thus imply that former traits could be reestablished with demographic recovery.publishedVersio

Ticket to spawn: Combining economic and genetic data to evaluate the effect of climate and demographic structure on spawning distribution in Atlantic cod

Climate warming and harvesting affect the dynamics of species across the globe through a multitude of mechanisms, including distribution changes. In fish, migrations to and distribution on spawning grounds are likely influenced by both climate warming and harvesting. The Northeast Arctic (NEA) cod (Gadus morhua) performs seasonal migrations from its feeding grounds in the Barents Sea to spawning grounds along the Norwegian coast. The distribution of cod between the spawning grounds has historically changed at decadal scales, mainly due to variable use of the northern and southern margins of the spawning area. Based on historical landing records, two major hypotheses have been put forward to explain these changes: climate and harvesting. Climate could affect the distribution through, for example, spatial habitat shifts. Harvesting could affect the distribution through impacting the demographic structure. If demographic structure is important, theory predicts increasing spawner size with migration distance. Here, we evaluate these hypotheses with modern data from a period (2000–2016) of increasing temperature and recovering stock structure. We first analyze economic data from the Norwegian fisheries to investigate geographical differences in size of spawning fish among spawning grounds, as well as interannual differences in mean latitude of spawning in relation to changes in temperature and demographic parameters. Second, we analyze genetically determined fish sampled at the spawning grounds to unambiguously separate between migratory NEA cod and potentially smaller sized coastal cod of local origin. Our results indicate smaller spawners farther away from the feeding grounds, hence not supporting the hypothesis that harvesting is a main driver for the contemporary spawning ground distribution. We find a positive correlation between annual mean spawning latitude and temperature. In conclusion, based on contemporary data, there is more support for climate compared to harvesting in shaping spawning ground distribution in this major fish stock in the North Atlantic Ocean