Demographic inferences after a range expansion can be biased: the test case of the blacktip reef shark (Carcharhinus melanopterus).

The evolutionary history of species is a dynamic process as they modify, expand, and contract their spatial distributions over time. Range expansions (REs) occur through a series of founder events that are followed by migration among neighboring demes. The process usually results in structured metapopulations and leaves a distinct signature in the genetic variability of species. Explicitly modeling the consequences of complex demographic events such as REs is computationally very intensive. Here we propose an an alternative approach that requires less computational effort than a comprehensive RE model, but that can recover the demography of species undergoing a RE, by combining spatially explicit modelling with simplified but realistic metapopulation models. We examine the demographic and colonization history of Carcharhinus melanopterus, an abundant reef-associated shark, as a test case. We first used a population genomics approach to statistically confirm the occurrence of a RE in C. melanopterus, and identify its origin in the Indo-Australian Archipelago. Spatial genetic modelling identified two waves of stepping-stone colonization: an eastward wave moving through the Pacific and a westward one moving through the Indian Ocean. We show that metapopulation models best describe the demographic history of this species and that not accounting for this may lead to incorrectly interpreting the observed genetic variation as signals of widespread population bottlenecks. Our study highlights insights that can be gained about demography by coupling metapopulation models with spatial modeling and underscores the need for cautious interpretation of population genetic data when advancing conservation priorities.

Chance, Variation and Shared Ancestry: Population Genetics After the Synthesis.

Chance has been a focus of attention ever since the beginning of population genetics, but neutrality has not, as natural selection once appeared to be the only worthwhile issue. Neutral change became a major source of interest during the neutralist-selectionist debate, 1970-1980. It retained interest beyond this period for two reasons that contributed to its becoming foundational for evolutionary reasoning. On the one hand, neutral evolution was the first mathematical prediction to emerge from Mendelian inheritance: until then evolution by natural selection was considered the alternative to the fixity of species; now it appears to be the alternative to continuous change. Second, neutral change generated a set of clear predictions on standing variation. These could be used as a reference for detecting more elusive alternative mechanisms of evolution including natural selection. In the wake of the transition from Mendelism to genomics, the combination of coalescent theory, DNA sequence variation, and numerical analysis made it possible to integrate contingent aspects of the history of species into a new null model, thus opening a new dimension in the concept of population that the Modern Synthesis formerly considered as a mere gene pool.

The population determines whether and how life-history traits vary between reproductive events in an insect with maternal care.

The last reproductive event of a female is often associated with major changes in terms of both maternal and offspring life-history traits. However, the nature of these changes and the importance of population-specific environmental constraints in shaping their expression are difficult to predict and, as a consequence, poorly understood. Here, we investigated whether and how life-history traits vary between reproductive events and whether this variation is population-dependent in the European earwig Forficula auricularia. In this insect species, females produce up to two clutches during their lifetime and express extensive forms of maternal care. We conducted a common garden experiment, in which we measured 11 life-history traits of the first and second clutches of 132 females originating from three populations. Our results showed that clutch size was higher and the level of care expressed towards juveniles lower in second as compared to the first clutches in all three populations. In contrast, we found a population-specific effect on whether and how the reproductive event shaped juvenile quality and a trade-off between egg developmental time and female weight at hatching. Overall, these findings emphasise that the last reproductive event of a female entails both positive and negative effects on various life-history traits of the female herself and her clutch of juveniles. Moreover, our study stresses the importance of population idiosyncrasies on the expression and nature of such cohort-specific effects.

Signatures of purifying and local positive selection in human miRNAs.

MicroRNAs (miRNAs) are noncoding RNAs involved in posttranscriptional gene repression, and their role in diverse physiological processes is increasingly recognized. Yet, few efforts have been devoted to evolutionary studies of human miRNAs. Knowledge about the way in which natural selection has targeted miRNAs should provide insight into their functional relevance as well as their mechanisms of action. Here we used miRNAs as a model system for investigating the influence of natural selection on gene regulation by characterizing the full spectrum of naturally occurring sequence variation of 117 human miRNAs from different populations worldwide. We found that purifying selection has globally constrained the diversity of miRNA-containing regions and has strongly targeted the mature miRNA. This observation emphasizes that mutations in these molecules are likely to be deleterious, and therefore they can have severe phenotypic consequences on human health. More importantly, we obtained evidence of population-specific events of positive selection acting on a number of miRNA-containing regions. Notably, our analysis revealed that positive selection has targeted a "small-RNA-rich island" on chromosome 14, harboring both miRNAs and small nucleolar RNAs, in Europeans and East Asians. These observations support the notion that the tuning of gene expression contributes to the processes by which populations adapt to specific environments. These findings will fuel future investigations exploring how genetic and functional variation of miRNAs under selection affects the repression of their mRNA targets, increasing our understanding of the role of gene regulation in population adaptation and human disease.

Lactase persistence in central Asia: phenotype, genotype, and evolution.

The aim of the present study is to document the evolution of the lactase persistence trait in Central Asia, a geographical area that is thought to have been a region of long-term pastoralism. Several ethnic groups co-exist in this area: Indo-Iranian speakers who are traditionally agriculturist (Tajik) and Turkic speakers who used to be nomadic herders (Kazakh, Karakalpak, Kyrgyz, Turkmen). It was recently demonstrated that horse milking practice existed in the Botai culture of Kazakhstan as early as 5,500 BP ( Outram et al. 2009 ). However, the frequency of the lactase persistence trait and its genetic basis in Central Asian populations remain largely unknown. We propose here the first genotype-phenotype study of lactase persistence in Central Asia based on 183 individuals, as well as the estimation of the time of expansion of the lactase-persistence associated polymorphism. Our results show a remarkable genetic-phenotypic correlation, with the causal polymorphism being the same than in Europe (-13.910C>T, rs4988235). The lactase persistence trait is at low frequency in these populations: between 25% and 32% in the Kazakh population (traditionally herders), according to phenotype used, and between 11% and 30% in the Tajiko-Uzbek population (agriculturalists). The difference in lactase persistence between populations, even if small, is significant when using individuals concordant for both excretion of breath hydrogen and the lactose tolerance blood glucose test phenotypes (P = 0.018, 25% for Kazakh vs. 11% for Tajiko-Uzbeks), and the difference in frequency of the -13.910*T allele is almost significant (P = 0.06, 30% for Kazakhs vs. 19% for Tajiko-Uzbeks). Using the surrounding haplotype, we estimate a date of expansion of the T allele around 6,000-12,000 yrs ago, which is consistent with archaeological records for the emergence of agropastoralism and pastoralism in Central Asia.

DNA barcode analysis: a comparison of phylogenetic and statistical classification methods.

BACKGROUND: DNA barcoding aims to assign individuals to given species according to their sequence at a small locus, generally part of the CO1 mitochondrial gene. Amongst other issues, this raises the question of how to deal with within-species genetic variability and potential transpecific polymorphism. In this context, we examine several assignation methods belonging to two main categories: (i) phylogenetic methods (neighbour-joining and PhyML) that attempt to account for the genealogical framework of DNA evolution and (ii) supervised classification methods (k-nearest neighbour, CART, random forest and kernel methods). These methods range from basic to elaborate. We investigated the ability of each method to correctly classify query sequences drawn from samples of related species using both simulated and real data. Simulated data sets were generated using coalescent simulations in which we varied the genealogical history, mutation parameter, sample size and number of species. RESULTS: No method was found to be the best in all cases. The simplest method of all, "one nearest neighbour", was found to be the most reliable with respect to changes in the parameters of the data sets. The parameter most influencing the performance of the various methods was molecular diversity of the data. Addition of genetically independent loci--nuclear genes--improved the predictive performance of most methods. CONCLUSION: The study implies that taxonomists can influence the quality of their analyses either by choosing a method best-adapted to the configuration of their sample, or, given a certain method, increasing the sample size or altering the amount of molecular diversity. This can be achieved either by sequencing more mtDNA or by sequencing additional nuclear genes. In the latter case, they may also have to modify their data analysis method.

Selective sweeps in a 2-locus model for sex-ratio meiotic drive in Drosophila simulans.

A way to identify loci subject to positive selection is to detect the signature of selective sweeps in given chromosomal regions. It is revealed by the departure of DNA polymorphism patterns from the neutral equilibrium predicted by coalescent theory. We surveyed DNA sequence variation in a region formerly identified as causing "sex-ratio" meiotic drive in Drosophila simulans. We found evidence that this system evolved by positive selection at 2 neighboring loci, which thus appear to be required simultaneously for meiotic drive to occur. The 2 regions are approximately 150-kb distant, corresponding to a genetic distance of 0.1 cM. The presumably large transmission advantage of chromosomes carrying meiotic drive alleles at both loci has not erased the individual signature of selection at each locus. This chromosome fragment combines a high level of linkage disequilibrium between the 2 critical regions with a high recombination rate. As a result, 2 characteristic traits of selective sweeps--the reduction of variation and the departure from selective neutrality in haplotype tests--show a bimodal pattern. Linkage disequilibrium level indicates that, in the natural population from Madagascar used in this study, the selective sweep may be as recent as 100 years.

Molecular taxonomy and species delimitation in Andean Schistocerca (Orthoptera: Acrididae).

The acridian genus Schistocerca comprises about 50 species which are endemic to the New World, except the Old World locust S. gregaria. Their morphological identification is rendered difficult by phase polyphenism, geographical overlap due to migrations or swarming, the difficulty to easily differentiate genitalia and the occurrence of interspecific hybrids. The three species reported from Peru include the swarming species S. interrita, a pest that can be recognized only by taxonomists. We show that it can be unambiguously identified using a mitochondrial DNA fragment known to have barcoding properties in this genus. We used several methods to delimitate Peruvian species. While S. interrita and S. pallens were well characterized, S. piceifrons peruviana was split into several taxa by a phylogeny-based method, whereas a combination of population genetics methods led one to identify only the three nominal species. A tentative reconstruction of the species history shows that several populations of S. piceifrons peruviana have recently increased in number, while exchanging some migrants, whereas an isolated population at the northern margin of the species range is substantially differentiated while exchanging no migrants with the others. This complex history has resulted in an atypical lineage pattern that appears to have confounded the standard assumptions underlying available species delimitation methods. Because of its behavioral property which tends to keep it panmictic, the identification of the swarming S. interrita remained unaffected.

A DNA barcode reference library of French Polynesian shore fishes.

The emergence of DNA barcoding and metabarcoding opened new ways to study biological diversity, however, the completion of DNA barcode libraries is fundamental for such approaches to succeed. This dataset is a DNA barcode reference library (fragment of Cytochrome Oxydase I gene) for 2,190 specimens representing at least 540 species of shore fishes collected over 10 years at 154 sites across the four volcanic archipelagos of French Polynesia; the Austral, Gambier, Marquesas and Society Islands, a 5,000,000 km2 area. At present, 65% of the known shore fish species of these archipelagoes possess a DNA barcode associated with preserved, photographed, tissue sampled and cataloged specimens, and extensive collection locality data. This dataset represents one of the most comprehensive DNA barcoding efforts for a vertebrate fauna to date. Considering the challenges associated with the conservation of coral reef fishes and the difficulties of accurately identifying species using morphological characters, this publicly available library is expected to be helpful for both authorities and academics in various fields.

Contrasted polymorphism patterns in a large sample of populations from the evolutionary genetics model Drosophila simulans.

African populations of Drosophila simulans are thought to be ancestral in this model species and are increasingly used for testing general hypotheses in evolutionary genetics. It is often assumed that African populations are more likely to be at a neutral mutation drift equilibrium than other populations. Here we examine population structuring and the demographic profile in nine populations of D. simulans. We surveyed sequence variation in four X-linked genes (runt, sevenless, Sex-lethal, and vermilion) that have been used in a parallel study in the closely related species D. melanogaster. We found that an eastern group of populations from continental Africa and Indian Ocean islands (Kenya, Tanzania, Madagascar, and Mayotte Island) is widespread, shows little differentiation, and has probably undergone demographic expansion. The other two African populations surveyed (Cameroon and Zimbabwe) show no evidence of population expansion and are markedly differentiated from each other as well as from the populations from the eastern group. Two other populations, Europe and Antilles, are probably recent invaders to these areas. The Antilles population is probably derived from Europe through a substantial bottleneck. The history of these populations should be taken into account when drawing general conclusions from variation patterns.

Population expansions dominate demographic histories of endemic and widespread Pacific reef fishes.

Despite the unique nature of endemic species, their origin and population history remain poorly studied. We investigated the population history of 28 coral reef fish species, close related, from the Gambier and Marquesas Islands, from five families, with range size varying from widespread to small-range endemic. We analyzed both mitochondrial and nuclear sequence data using neutrality test and Bayesian analysis (EBSP and ABC). We found evidence for demographic expansions for most species (24 of 28), irrespective of range size, reproduction strategy or archipelago. The timing of the expansions varied greatly among species, from 8,000 to 2,000,000 years ago. The typical hypothesis for reef fish that links population expansions to the Last Glacial Maximum fit for 14 of the 24 demographic expansions. We propose two evolutionary processes that could lead to expansions older than the LGM: (a) we are retrieving the signature of an old colonization process for widespread, large-range endemic and paleoendemic species or (b) speciation; the expansion reflects the birth of the species for neoendemic species. We show for the first time that the demographic histories of endemic and widespread reef fish are not distinctly different and suggest that a number of processes drive endemism.

Population genomics of C. melanopterus using target gene capture data: demographic inferences and conservation perspectives.

Population genetics studies on non-model organisms typically involve sampling few markers from multiple individuals. Next-generation sequencing approaches open up the possibility of sampling many more markers from fewer individuals to address the same questions. Here, we applied a target gene capture method to deep sequence ~1000 independent autosomal regions of a non-model organism, the blacktip reef shark (Carcharhinus melanopterus). We devised a sampling scheme based on the predictions of theoretical studies of metapopulations to show that sampling few individuals, but many loci, can be extremely informative to reconstruct the evolutionary history of species. We collected data from a single deme (SID) from Northern Australia and from a scattered sampling representing various locations throughout the Indian Ocean (SCD). We explored the genealogical signature of population dynamics detected from both sampling schemes using an ABC algorithm. We then contrasted these results with those obtained by fitting the data to a non-equilibrium finite island model. Both approaches supported an Nm value ~40, consistent with philopatry in this species. Finally, we demonstrate through simulation that metapopulations exhibit greater resilience to recent changes in effective size compared to unstructured populations. We propose an empirical approach to detect recent bottlenecks based on our sampling scheme.

Ancient balancing selection at tan underlies female colour dimorphism in Drosophila erecta.

Dimorphic traits are ubiquitous in nature, but the evolutionary factors leading to dimorphism are largely unclear. We investigate a potential case of sexual mimicry in Drosophila erecta, in which females show contrasting resemblance to males. We map the genetic basis of this sex-limited colour dimorphism to a region containing the gene tan. We find a striking signal of ancient balancing selection at the 'male-specific enhancer' of tan, with exceptionally high sequence divergence between light and dark alleles, suggesting that this dimorphism has been adaptively maintained for millions of years. Using transgenic reporter assays, we confirm that these enhancer alleles encode expression differences that are predicted to generate this pigmentation dimorphism. These results are compatible with the theoretical prediction that divergent phenotypes maintained by selection can evolve simple genetic architectures.

Effect of breeding structure on population genetic parameters in Drosophila.

The breeding structure of populations has been neglected in studies of Drosophila, even though Wright and Dobzhansky's pioneering work on the genetics of natural populations was an attempt to tackle what they regarded as an essential factor in evolution. We compared the breeding structure of sympatric populations of D. melanogaster and D. simulans, two sibling species that are widely used in evolutionary studies. We recorded changes in population density and microsatellite variation patterns for 3 years in a temperate environment of southwestern France. Results were distinctively different in the two species. Maximum population levels in summer and in autumn were similar and fluctuated greatly over years, each species being in turn the most abundant. However, genetic data showed that D. melanogaster made up a continuous breeding population in time and space of practically infinite effective size. D. simulans was fragmented into isolates with a local effective size of between 50 and 350 individuals. A consequence of this was that, while a local sample provided a reliable estimate of regional genetic variability in D. melanogaster, a sample from the same area provided an underestimate of this parameter in D. simulans. In practical terms, this means that variations in breeding structure should be accounted for in sampling schemes and in designing evolutionary genetic models. More generally, this suggests the existence of differential reactions to local environments that might contribute to several genomic differences observed between these species.

Signature of selective sweep associated with the evolution of sex-ratio drive in Drosophila simulans.

In several Drosophila species, the XY Mendelian ratio is disturbed by X-linked segregation distorters (sex-ratio drive). We used a collection of recombinants between a nondistorting chromosome and a distorting X chromosome originating from the Seychelles to map a candidate sex-ratio region in Drosophila simulans using molecular biallelic markers. Our data were compatible with the presence of a sex-ratio locus in the 7F cytological region. Using sequence polymorphism at the Nrg locus, we showed that sex-ratio has induced a strong selective sweep in populations from Madagascar and Réunion, where distorting chromosomes are close to a 50% frequency. The complete association between the marker and the sex-ratio phenotype and the near absence of mutations and recombination in the studied fragment after the sweep event indicate that this event is recent. Examples of selective sweeps are increasingly reported in a number of genomes. This case identifies the causal selective force. It illustrates that all selective sweeps are not necessarily indicative of an increase in the average fitness of populations.

Evidence of a high rate of selective sweeps in African Drosophila melanogaster.

Assessing the rate of evolution depends on our ability to detect selection at several genes simultaneously. We summarize DNA sequence variation data in three new and six previously published data sets from the left arm of the second chromosome of Drosophila melanogaster in a population from West Africa, the presumed area of origin of this species. Four loci [Acp26Aa, Fbp2, Vha68-1, and Su(H)] were previously found to deviate from a neutral mutation-drift equilibrium as a consequence of one or several selective sweeps. Polymorphism data from five loci from intervening regions (dpp, Acp26Ab, Acp29AB, GH10711, and Sos) did not show the characteristic deviation from neutrality caused by local selective sweeps. This genomic region is polymorphic for the In(2L)t inversion. Four loci located near inversion breakpoints [dpp, sos, GH10711, and Su(H)] showed significant structuring between the two arrangements or significant deviation from neutrality in the inverted class, probably as a result of a recent shift in inversion frequency. Overall, these patterns of variation suggest that the four selective events were independent. Six loci were observed with no a priori knowledge of selection, and independent selective sweeps were detected in three of them. This suggests that a large part of the D. melanogaster genome has experienced the effect of positive selection in its ancestral African range.

Investigating sex-specific dynamics using uniparental markers: West New Guinea as a case study.

Mitochondrial DNA (mtDNA) and Y chromosome (NRY) genetic markers have been often contrasted to investigate sex-specific dynamics. Traditionally, isolation by distance, intrapopulation genetic diversity and population differentiation are estimated from both markers and compared. Two possible sources of bias are often neglected. First, kilometric distances are frequently used as predictor of the connectivity between groups, hiding the role played by environmental features at a microgeographic scale. Second, the comparison of intrapopulation diversity and population differentiation between mtDNA and NRY is hampered by their different mutational mechanisms and rates. Here, we show how to account for these biases by analyzing from a different perspective a published dataset of eight West New Guinea (WNG) populations for which mtDNA control region sequences and seven linked NRY microsatellites had been typed. First, we modeled the connectivity among sampled populations by computing the number of days required to travel between groups. Then, we investigated the differences between the two sexes accounting for the molecular characteristics of the markers examined to obtain estimates on the product of the effective population size and the migration rate among demes (Nm). We achieved this goal by studying the shape of the gene genealogy at several sampling levels and using spatial explicit simulations. Both the direction and the rate of migration differ between male and females, with an Nm estimated to be >6 times higher in the latter under many evolutionary scenarios. We finally highlight the importance of applying metapopulation models when analyzing the genetic diversity of a species. We have applied the prediction of the sampling theory in a meta-population and we have corroborated our finding using spatial explicit simulations. Both approaches are fundamentally meant to deal with structured populations: we strongly believe in the importance of tacking structure into account when inferring the demographic history of a species.

Phylogenetic analyses of mitochondrial and nuclear data in haematophagous flies support the paraphyly of the genus Stomoxys (Diptera: Muscidae).

The genus Stomoxys Geoffroy (Diptera; Muscidae) contains species of parasitic flies that are of medical and economic importance. We conducted a phylogenetic analysis including 10 representative species of the genus including multiple exemplars, together with the closely related genera Prostomoxys Zumpt, Haematobosca Bezzi, and Haematobia Lepeletier & Serville. Phylogenetic relationships were inferred using maximum likelihood and Bayesian methods from DNA fragments from the cytochrome c oxidase subunit I (COI, 753bp) and cytochrome b (CytB, 587bp) mitochondrial genes, and the nuclear ribosomal internal transcribed spacer 2 (ITS2, 426bp). The combination of mitochondrial and nuclear data strongly supports the paraphyly of the genus Stomoxys because of the inclusion of Prostomoxys saegerae Zumpt. This unexpected result suggests that Prostomoxys should be renamed into Stomoxys. Also, the deep molecular divergence observed between the subspecies Stomoxys niger niger Macquart and S. niger bilineatus Grünbreg led us to propose that they should rather be considered as distinct species, in agreement with ecological data. Bayesian phylogenetic analyses support three distinct lineages within the genus Stomoxys with a strong biogeographical component. The first lineage consists solely of the divergent Asian species S. indicus Picard which appears as the sister-group to all remaining Stomoxys species. The second clade groups the strictly African species Stomoxys inornatus Grünbreg, Stomoxys transvittatus Villeneuve, Stomoxys omega Newstead, and Stomoxys pallidus Roubaud. Finally, the third clade includes both African occurring and more widespread species such as the livestock pest Stomoxys calcitrans Linnaeus. Divergence time estimates indicate that the genus Stomoxys originated in the late Oligocene around 30 million years ago, with the major lineages diversifying in the Early Miocene between 20 and 15 million years ago at a time when temperate forests developed in the Northern Hemisphere.

Darwin and sexual selection: One hundred years of misunderstanding.

Darwin's book on the Descent of Man and Selection in Relation to Sex (1871) is often viewed as the continuation of The Origin of Species published 12 years earlier (1859), both because of the implicit parallelism between natural selection and sexual selection, and because Darwin himself presents the book as developing a subject (man) which he intentionally omitted in the Origin. But the Descent can also be viewed as the continuation of his book on Variation published three years earlier (1868). Firstly because Darwin's hypothesis of pangenesis links the selection process to the origin of variation through use and disuse, an idea underlying his speculations on the origin of moral sense in humans. Second because like the action of the horticulturist on his domestic crops, sexual selection exerted by one sex on the other sex can develop fancy traits that are not easily accounted for by their utility to the selected organism itself, such as artistic taste, pride, courage, and the morphological differences between human populations. These traits are difficult to reconcile with pangenesis. They add up to other contradictions of the book possibly resulting from Darwin's erroneous inference about the mechanism of inheritance, like those on the determination of sex-ratio, or the confusion between individual adaptation and the advantage to the species. These inconsistencies inaugurate a weakening of the Darwinian message, which will last 50 years after his death. They contributed to the neglect of sexual selection for a century. Darwin however maintained a logical distinction between evolutionary mechanisms and hereditary mechanisms, and an epistemological distinction between evolutionary theory and Pangenesis hypothesis. In the modern context of Mendelian genetics, Darwin's sexual selection retrospectively appears as luminous an idea in its pure principle as natural selection, even though the mechanisms governing the evolution of sexual choice in animals remain largely unresolved.