Maarten Larmuseau

Divergent selection as revealed by P(ST) and QTL-based F(ST) in three-spined stickleback (Gasterosteus aculeatus) populations along a coastal-inland gradient

Three measures of divergence, estimated at nine putatively neutral microsatellite markers, 14 quantitative traits, and seven quantitative trait loci (QTL) were compared in eight populations of the three‐spined stickleback (Gasterosteus aculeatus L.) living in the Scheldt river basin (Belgium). Lowland estuarine and polder populations were polymorphic for the number of lateral plates, whereas upland freshwater populations were low‐plated. The number of short gill rakers and the length of dorsal and pelvic spines gradually declined along a coastal‐inland gradient. Plate number, short gill rakers and spine length showed moderate to strong signals of divergent selection between lowland and upland populations in comparison between PST (a phenotypic alternative for QST) and neutral FST. However, such comparisons rely on the unrealistic assumption that phenotypic variance equals additive genetic variance, and that nonadditive genetic effects and environmental effects can be minimized. In order to verify this assumption and to confirm the phenotypic signals of divergence, we tested for divergent selection at the underlying QTL. For plate number, strong genetic evidence for divergent selection between lowland and upland populations was obtained based on an intron marker of the Eda gene, of which the genotype was highly congruent with plate morph. Genetic evidence for divergent selection on short gill rakers was limited to some population pairs where FST at only one of two QTL was detected as an outlier, although FST at both loci correlated significantly with PST. No genetic confirmation was obtained for divergent selection on dorsal spine length, as no outlier FSTs were detected at dorsal spine QTL, and no significant correlations with PST were observed.

Seeing the wood for the trees: a minimal reference phylogeny for the human Y chromosome.

During the last few decades, a wealth of studies dedicated to the human Y chromosome and its DNA variation, in particular Y‐chromosome single‐nucleotide polymorphisms (Y‐SNPs), has led to the construction of a well‐established Y‐chromosome phylogeny. Since the recent advent of new sequencing technologies, the discovery of additional Y‐SNPs is exploding and their continuous incorporation in the phylogenetic tree is leading to an ever higher resolution. However, the large and increasing amount of information included in the “complete” Y‐chromosome phylogeny, which now already includes many thousands of identified Y‐SNPs, can be overwhelming and complicates its understanding as well as the task of selecting suitable markers for genotyping purposes in evolutionary, demographic, anthropological, genealogical, medical, and forensic studies. As a solution, we introduce a concise reference phylogeny whereby we do not aim to provide an exhaustive tree that includes all known Y‐SNPs but, rather, a quite stable reference tree aiming for optimal global discrimination capacity based on a strongly reduced set that includes only the most resolving Y‐SNPs. Furthermore, with this reference tree, we wish to propose a common standard for Y‐marker as well as Y‐haplogroup nomenclature. The current version of our tree is based on a core set of 417 branch‐defining Y‐SNPs and is available online at http://www.phylotree.org/Y.

The Y-Chromosome Tree Bursts into Leaf: 13,000 High-Confidence SNPs Covering the Majority of Known Clades

Many studies of human populations have used the male-specific region of the Y chromosome (MSY) as a marker, but MSY sequence variants have traditionally been subject to ascertainment bias. Also, dating of haplogroups has relied on Y-specific short tandem repeats (STRs), involving problems of mutation rate choice, and possible long-term mutation saturation. Next-generation sequencing can ascertain single nucleotide polymorphisms (SNPs) in an unbiased way, leading to phylogenies in which branch-lengths are proportional to time, and allowing the times-to-most-recent-common-ancestor (TMRCAs) of nodes to be estimated directly. Here we describe the sequencing of 3.7 Mb of MSY in each of 448 human males at a mean coverage of 51×, yielding 13,261 high-confidence SNPs, 65.9% of which are previously unreported. The resulting phylogeny covers the majority of the known clades, provides date estimates of nodes, and constitutes a robust evolutionary framework for analyzing the history of other classes of mutation. Different clades within the tree show subtle but significant differences in branch lengths to the root. We also apply a set of 23 Y-STRs to the same samples, allowing SNP- and STR-based diversity and TMRCA estimates to be systematically compared. Ongoing purifying selection is suggested by our analysis of the phylogenetic distribution of nonsynonymous variants in 15 MSY single-copy genes.

Mito-nuclear discordance in the degree of population differentiation in a marine goby

An increasing number of phylogeographic studies on marine species shows discordant patterns in the degree of population differentiation between nuclear and mitochondrial markers. To understand better which factors have the potential to cause these patterns of discordance in marine organisms, a population genetic study was realized on the sand goby Pomatoschistus minutus (Pallas 1770; Gobiidae, Teleostei). Sand gobies from eight European locations were genotyped at eight microsatellite markers. Microsatellites confirmed the global phylogeographical pattern of P. minutus observed with mitochondrial DNA (mtDNA) markers and nuclear allozyme markers. Three groups consistent with the mitochondrial lineages were defined (the Mediterranean, Iberian and North Atlantic groups) and indications of a recent founder event in the northern Baltic Sea were found. Nevertheless, differences in the degree of population differentiation between the nuclear and mitochondrial markers were large (global FST-values for microsatellites=0.0121; for allozymes=0.00831; for mtDNA=0.4293). Selection, sex-biased dispersal, homoplasy and a high effective population size are generally accepted as explanations for this mitonuclear discrepancy in the degree of population differentiation. In this study, selection on mtDNA and microsatellites, male-biased dispersal and homoplasy on microsatellite markers are unlikely to be a main cause for this discrepancy. The most likely reason for the discordant pattern is a recent demographical expansion of the sand goby, resulting in high effective population sizes slowing down the differentiation of nuclear DNA.

Temporal genetic stability and high effective population size despite fisheries-induced life-history trait evolution in the North Sea sole.

Heavy fishing and other anthropogenic influences can have profound impact on a species’ resilience to harvesting. Besides the decrease in the census and effective population size, strong declines in mature adults and recruiting individuals may lead to almost irreversible genetic changes in life‐history traits. Here, we investigated the evolution of genetic diversity and effective population size in the heavily exploited sole (Solea solea), through the analysis of historical DNA from a collection of 1379 sole otoliths dating back from 1957. Despite documented shifts in life‐history traits, neutral genetic diversity inferred from 11 microsatellite markers showed a remarkable stability over a period of 50 years of heavy fishing. Using simulations and corrections for fisheries induced demographic variation, both single‐sample estimates and temporal estimates of effective population size (Ne) were always higher than 1000, suggesting that despite the severe census size decrease over a 50‐year period of harvesting, genetic drift is probably not strong enough to significantly decrease the neutral diversity of this species in the North Sea. However, the inferred ratio of effective population size to the census size (Ne/Nc) appears very small (10−5), suggesting that overall only a low proportion of adults contribute to the next generation. The high Ne level together with the low Ne/Nc ratio is probably caused by a combination of an equalized reproductive output of younger cohorts, a decrease in generation time and a large variance in reproductive success typical for marine species. Because strong evolutionary changes in age and size at first maturation have been observed for sole, changes in adaptive genetic variation should be further monitored to detect the evolutionary consequences of human‐induced selection.

AMY-tree: an algorithm to use whole genome SNP calling for Y chromosomal phylogenetic applications

BackgroundDue to the rapid progress of next-generation sequencing (NGS) facilities, an explosion of human whole genome data will become available in the coming years. These data can be used to optimize and to increase the resolution of the phylogenetic Y chromosomal tree. Moreover, the exponential growth of known Y chromosomal lineages will require an automatic determination of the phylogenetic position of an individual based on whole genome SNP calling data and an up to date Y chromosomal tree.ResultsWe present an automated approach, ‘AMY-tree’, which is able to determine the phylogenetic position of a Y chromosome using a whole genome SNP profile, independently from the NGS platform and SNP calling program, whereby mistakes in the SNP calling or phylogenetic Y chromosomal tree are taken into account. Moreover, AMY-tree indicates ambiguities within the present phylogenetic tree and points out new Y-SNPs which may be phylogenetically relevant. The AMY-tree software package was validated successfully on 118 whole genome SNP profiles of 109 males with different origins. Moreover, support was found for an unknown recurrent mutation, wrong reported mutation conversions and a large amount of new interesting Y-SNPs.ConclusionsTherefore, AMY-tree is a useful tool to determine the Y lineage of a sample based on SNP calling, to identify Y-SNPs with yet unknown phylogenetic position and to optimize the Y chromosomal phylogenetic tree in the future. AMY-tree will not add lineages to the existing phylogenetic tree of the Y-chromosome but it is the first step to analyse whole genome SNP profiles in a phylogenetic framework.

Differential modes of selection on the rhodopsin gene in coastal Baltic and North Sea populations of the sand goby, Pomatoschistus minutus

An excellent model to elucidate the mechanisms and importance of evolution in the marine environment is the spectral tuning mechanism of the visual pigment in vertebrates. In the sand goby Pomatoschistus minutus (Teleostei; Gobiidae), a distribution‐wide study showed that spatial variation at the rhodopsin gene (RH1) matches the characteristics of specific light environments. This match suggests that populations are locally adapted to selective light regimes targeting the RH1 gene. If so, then the direction of selection should depend on the regional spatial and temporal stability of the light conditions. We tested this prediction by comparing goby populations from two regions: the Baltic Sea, characterized by divergent, but temporally stable light conditions, and the North Sea, characterized by locally heterogeneous and temporally variable light conditions. RH1 sequences of 491 Pomatoschistus minutus individuals from 15 locations were analysed. We found that variation at the RH1 gene in the Baltic populations showed signatures of diversifying selection, whereas the RH1 gene in the North Sea showed signatures of stabilizing selection. These different modes of selection are consistent with the regional light conditions and hence support our predictions, but may also be influenced by migration between the open sea and more turbid estuarine environments. An interesting observation is that within one gene, synonymous and non‐synonymous SNPs show a totally different pattern between populations. Population differentiation based on non‐synonymous SNPs of the RH1 gene correlated with spectral variation of the local environment of the sand goby populations. In contrast, the differentiation based on synonymous SNPs of RH1 reflects more the neutral historical pattern of the species.

Low historical rates of cuckoldry in a Western European human population traced by Y-chromosome and genealogical data

Recent evidence suggests that seeking out extra-pair paternity (EPP) can be a viable alternative reproductive strategy for both males and females in many pair-bonded species, including humans. Accurate data on EPP rates in humans, however, are scant and mostly restricted to extant populations. Here, we provide the first large-scale, unbiased genetic study of historical EPP rates in a Western European human population based on combining Y-chromosomal data to infer genetic patrilineages with genealogical and surname data, which reflect known historical presumed paternity. Using two independent methods, we estimate that over the last few centuries, EPP rates in Flanders (Belgium) were only around 1–2% per generation. This figure is substantially lower than the 8–30% per generation reported in some behavioural studies on historical EPP rates, but comparable with the rates reported by other genetic studies of contemporary Western European populations. These results suggest that human EPP rates have not changed substantially during the last 400 years in Flanders and imply that legal genealogies rarely differ from the biological ones. This result has significant implications for a diverse set of fields, including human population genetics, historical demography, forensic science and human sociobiology.

Micro-geographic distribution of Y-chromosomal variation in the central-western European region Brabant

One of the future issues in the forensic application of the haploid Y-chromosome (Y-chr) is surveying the distribution of the Y-chr variation on a micro-geographical scale. Studies on such a scale require observing Y-chr variation on a high resolution, high sampling efforts and reliable genealogical data of all DNA-donors. In the current study we optimised this framework by surveying the micro-geographical distribution of the Y-chr variation in the central-western European region named Brabant. The Duchy of Brabant was a historical region in the Low Countries containing three contemporary Belgian provinces and one Dutch province (Noord-Brabant). 477 males from five a priori defined regions within Brabant were selected based on their genealogical ancestry (known pedigree at least before 1800). The Y-haplotypes were determined based on 37 Y-STR loci and the finest possible level of substructuring was defined according to the latest published Y-chr phylogenetic tree. In total, eight Y-haplogroups and 32 different subhaplogroups were observed, whereby 70% of all participants belonged to only four subhaplogroups: R1b1b2a1 (R-U106), R1b1b2a2* (R-P312*), R1b1b2a2g (R-U152) and I1* (I-M253*). Significant micro-geographical differentiation within Brabant was detected between the Dutch (Noord-Brabant) vs. the Flemish regions based on the differences in (sub)haplogroup frequencies but not based on Y-STR variation within the main subhaplogroups. A clear gradient was found with higher frequencies of R1b1b2 (R-M269) chromosomes in the northern vs. southern regions, mainly related to a trend in the frequency of R1b1b2a1 (R-U106).

Rapid range expansion increases genetic differentiation while causing limited reduction in genetic diversity in a damselfly

Many ectothermic species are currently expanding their geographic range due to global warming. This can modify the population genetic diversity and structure of these species because of genetic drift during the colonization of new areas. Although the genetic signatures of historical range expansions have been investigated in an array of species, the genetic consequences of natural, contemporary range expansions have received little attention, with the only studies available focusing on range expansions along a narrow front. We investigate the genetic consequences of a natural range expansion in the Mediterranean damselfly Coenagrion scitulum, which is currently rapidly expanding along a broad front in different directions. We assessed genetic diversity and genetic structure using 12 microsatellite markers in five centrally located populations and five recently established populations at the edge of the geographic distribution. Our results suggest that, although a marginal significant decrease in the allelic richness was found in the edge populations, genetic diversity has been preserved during the range expansion of this species. Nevertheless, edge populations were genetically more differentiated compared with core populations, suggesting genetic drift during the range expansion. The smaller effective population sizes of the edge populations compared with central populations also suggest a contribution of genetic drift after colonization. We argue and document that range expansion along multiple axes of a broad expansion front generates little reduction in genetic diversity, yet stronger differentiation of the edge populations.