Evolution of sex chromosomes prior to speciation in the dioecious Phoenix species.

Understanding the driving forces and molecular processes underlying dioecy and sex chromosome evolution, leading from hermaphroditism to the occurrence of male and female individuals, is of considerable interest in fundamental and applied research. The genus Phoenix, belonging to the Arecaceae family, consists uniquely of dioecious species. Phylogenetic data suggest that the genus Phoenix has diverged from a hermaphroditic ancestor which is also shared with its closest relatives. We have investigated the cessation of recombination in the sex-determination region within the genus Phoenix as a whole by extending the analysis of P. dactylifera SSR sex-related loci to eight other species within the genus. Phylogenetic analysis of a date palm sex-linked PdMYB1 gene in these species has revealed that sex-linked alleles have not clustered in a species-dependent way but rather in X and Y-allele clusters. Our data show that sex chromosomes evolved from a common autosomal origin before the diversification of the extant dioecious species.

Genomic signature of successful colonization of Eurasia by the allopolyploid shepherd's purse (Capsella bursa-pastoris).

Polyploidization is a dominant feature of flowering plant evolution. However, detailed genomic analyses of the interpopulation diversification of polyploids following genome duplication are still in their infancy, mainly because of methodological limits, both in terms of sequencing and computational analyses. The shepherd's purse (Capsella bursa-pastoris) is one of the most common weed species in the world. It is highly self-fertilizing, and recent genomic data indicate that it is an allopolyploid, resulting from hybridization between the ancestors of the diploid species Capsella grandiflora and Capsella orientalis. Here, we investigated the genomic diversity of C. bursa-pastoris, its population structure and demographic history, following allopolyploidization in Eurasia. To that end, we genotyped 261 C. bursa-pastoris accessions spread across Europe, the Middle East and Asia, using genotyping-by-sequencing, leading to a total of 4274 SNPs after quality control. Bayesian clustering analyses revealed three distinct genetic clusters in Eurasia: one cluster grouping samples from Western Europe and Southeastern Siberia, the second one centred on Eastern Asia and the third one in the Middle East. Approximate Bayesian computation (ABC) supported the hypothesis that C. bursa-pastoris underwent a typical colonization history involving low gene flow among colonizing populations, likely starting from the Middle East towards Europe and followed by successive human-mediated expansions into Eastern Asia. Altogether, these findings bring new insights into the recent multistage colonization history of the allotetraploid C. bursa-pastoris and highlight ABC and genotyping-by-sequencing data as promising but still challenging tools to infer demographic histories of selfing allopolyploids.

Comparative population genomics in animals uncovers the determinants of genetic diversity.

Genetic diversity is the amount of variation observed between DNA sequences from distinct individuals of a given species. This pivotal concept of population genetics has implications for species health, domestication, management and conservation. Levels of genetic diversity seem to vary greatly in natural populations and species, but the determinants of this variation, and particularly the relative influences of species biology and ecology versus population history, are still largely mysterious. Here we show that the diversity of a species is predictable, and is determined in the first place by its ecological strategy. We investigated the genome-wide diversity of 76 non-model animal species by sequencing the transcriptome of two to ten individuals in each species. The distribution of genetic diversity between species revealed no detectable influence of geographic range or invasive status but was accurately predicted by key species traits related to parental investment: long-lived or low-fecundity species with brooding ability were genetically less diverse than short-lived or highly fecund ones. Our analysis demonstrates the influence of long-term life-history strategies on species response to short-term environmental perturbations, a result with immediate implications for conservation policies.

Mating systems and selection efficacy: a test using chloroplastic sequence data in Angiosperms.

Selfing is assumed to reduce selection efficacy, especially purifying selection. This can be tested using molecular data, for example by comparing the Dn/Ds ratio between selfing and outcrossing lineages. So far, little evidence of relaxed selection against weakly deleterious mutations (as inferred by a higher Dn/Ds ratio) in selfers as compared to outcrossers has been found, contrary to the pattern often observed between asexual and sexual lineages. However, few groups have been studied to date. To further test this hypothesis, we compiled and analysed chloroplastic sequence data sets in several plant groups. We found a general trend towards relaxed selection in selfers in our data sets but with weak statistical support. Simulations suggested that the results were compatible with weak-to-moderate Dn/Ds ratio differences in selfing lineages. Simple theoretical predictions also showed that the ability to detect relaxed selection in selfers could strongly depend on the distribution of the effects of deleterious mutations on fitness. Our results are compatible with a recent origin of selfing lineages whereby deleterious mutations potentially have a strong impact on population extinction or with a more ancient origin but without a marked effect of deleterious mutations on the extinction dynamics.

Patterns of molecular evolution in dioecious and non-dioecious Silene.

Dioecy (i.e. having separate sexes) is a rather rare breeding system in flowering plants. Such rareness may result from a high probability of extinction in dioecious species because of less efficient dispersal and the costs of sexual selection, which are expected to harm dioecious species' survival on the long term. These handicaps should decrease the effective population size (Ne) of dioecious species, which in turn should reduce the efficacy of selection. Moreover, sexual selection in dioecious species is expected to specifically affect some genes, which will evolve under positive selection. The relative contribution of these effects is currently unknown and we tried to disentangle them by comparing sequence evolution between dioecious and non-dioecious species in the Silene genus (Caryophyllaceae), where dioecy has evolved at least twice. For the dioecious species in the section Melandrium, where dioecy is the oldest, we found a global reduction of purifying selection, while on some, male-biased genes, positive selection was found. For section Otites, where dioecy evolved more recently, we found no significant differences between dioecious and non-dioecious species. Our results are consistent with the view that dioecy is an evolutionary dead end in flowering plants, although other scenarios for explaining reduced Ne cannot be ruled out. Our results also show that contrasting forces act on the genomes of dioecious plants, and suggest that some time is required before the genome of such plants bears the footprints of dioecy.

The determinants of the molecular substitution process in turtles.

Neutral rates of molecular evolution vary across species, and this variation has been shown to be related to biological traits. One of the first patterns to be observed in vertebrates has been an inverse relationship between body mass (BM) and substitution rates. The effects of three major life-history traits (LHT) that covary with BM - metabolic rate, generation time and longevity (LON) - have been invoked to explain this relationship. However, most of the theoretical and empirical evidence supporting this relationship comes from endothermic vertebrates, that is, mammals and birds, in which the environmental conditions, especially temperature, do not have a direct impact on cellular and molecular biology. We analysed the variations in mitochondrial and nuclear rates of synonymous substitution across 224 turtle species and examined their correlation with two LHT (LON and BM) and two environmental variables [latitude (LAT) and habitat]. Our analyses indicate that in turtles, neutral rates of molecular evolution are hardly correlated with LON or BM. Rather, both the mitochondrial and nuclear substitution rates are significantly correlated with LAT - faster evolution in the tropics - and especially so for aquatic species. These results question the generality of the relationships reported in mammals and birds and suggest that environmental factors might be the strongest determinants of the mutation rate in ectotherms.

Mitochondrial DNA as a marker of molecular diversity: a reappraisal.

Over the last three decades, mitochondrial DNA has been the most popular marker of molecular diversity, for a combination of technical ease-of-use considerations, and supposed biological and evolutionary properties of clonality, near-neutrality and clock-like nature of its substitution rate. Reviewing recent literature on the subject, we argue that mitochondrial DNA is not always clonal, far from neutrally evolving and certainly not clock-like, questioning its relevance as a witness of recent species and population history. We critically evaluate the usage of mitochondrial DNA for species delineation and identification. Finally, we note the great potential of accumulating mtDNA data for evolutionary and functional analysis of the mitochondrial genome.

Mating system and recombination affect molecular evolution in four Triticeae species.

Mating systems and recombination are thought to have a deep impact on the organization and evolution of genomes. Because of the decline in effective population size and the interference between linked loci, the efficacy of selection is expected to be reduced in regions with low recombination rates and in the whole genome of self-fertilizing species. At the molecular level, relaxed selection is expected to result in changes in the rate of protein evolution and the pattern of codon bias. It is increasingly recognized that recombination also affects non-selective processes such as the biased gene conversion towards GC alleles (bGC). Like selection, this kind of meiotic drive in favour of GC over AT alleles is expected to be reduced in weakly recombining regions and genomes. Here, we investigated the effect of mating system and recombination on molecular evolution in four Triticeae species: two outcrossers (Secale cereale and Aegilops speltoides) and two selfers (Triticum urartu and Triticum monococcum). We found that GC content, possibly driven by bGC, is affected by mating system and recombination as theoretically predicted. Selection efficacy, however, is only weakly affected by mating system and recombination. We investigated the possible reasons for this discrepancy. A surprising one is that, in outcrossing lineages, selection efficacy could be reduced because of high substitution rates in favour of GC alleles. Outcrossers, but not selfers, would thus suffer from a 'GC-induced' genetic load. This result sheds new light on the evolution of mating systems.

Grinding up wheat: a massive loss of nucleotide diversity since domestication.

Several demographic and selective events occurred during the domestication of wheat from the allotetraploid wild emmer (Triticum turgidum ssp. dicoccoides). Cultivated wheat has since been affected by other historical events. We analyzed nucleotide diversity at 21 loci in a sample of 101 individuals representing 4 taxa corresponding to representative steps in the recent evolution of wheat (wild, domesticated, cultivated durum, and bread wheats) to unravel the evolutionary history of cultivated wheats and to quantify its impact on genetic diversity. Sequence relationships are consistent with a single domestication event and identify 2 genetically different groups of bread wheat. The wild group is not highly polymorphic, with only 212 polymorphic sites among the 21,720 bp sequenced, and, during domestication, diversity was further reduced in cultivated forms--by 69% in bread wheat and 84% in durum wheat--with considerable differences between loci, some retaining no polymorphism at all. Coalescent simulations were performed and compared with our data to estimate the intensity of the bottlenecks associated with domestication and subsequent selection. Based on our 21-locus analysis, the average intensity of domestication bottleneck was estimated at about 3--giving a population size for the domesticated form about one third that of wild dicoccoides. The most severe bottleneck, with an intensity of about 6, occurred in the evolution of durum wheat. We investigated whether some of the genes departed from the empirical distribution of most loci, suggesting that they might have been selected during domestication or breeding. We detected a departure from the null model of demographic bottleneck for the hypothetical gene HgA. However, the atypical pattern of polymorphism at this locus might reveal selection on the linked locus Gsp1A, which may affect grain softness--an important trait for end-use quality in wheat.

Marker-based investigation of inbreeding depression in the endangered species Brassica insularis.

Various methods have been proposed to estimate inbreeding depression and to assess its consequences for natural populations. As an alternative to controlled crosses, the use of molecular markers has allowed direct investigation of inbreeding depression in natural populations, but usually suffers from low statistical power. Here, we investigated the effect of inbreeding depression on survival in two populations of the rare species Brassica insularis, using both controlled crosses and a marker-based approach. We compare the respective merits of the two approaches for studying inbreeding depression. We also use information from the molecular markers to dissect in detail patterns of inbreeding depression in this species. A posteriori, we find that combining the approaches was not necessary to obtain simple point estimates of inbreeding depression. However, using molecular markers may give insight into the genetic basis of inbreeding depression, such as the occurrence of epistatic interactions among deleterious alleles or purging.

Inbreeding depression in small populations of self-incompatible plants.

Self-incompatibility (SI) is a widespread mechanism that prevents inbreeding in flowering plants. In many species, SI is controlled by a single locus (the S locus) where numerous alleles are maintained by negative frequency-dependent selection. Inbreeding depression, the decline in fitness of selfed individuals compared to outcrossed ones, is an essential factor in the evolution of SI systems. Conversely, breeding systems influence levels of inbreeding depression. Little is known about the joint effect of SI and drift on inbreeding depression. Here we studied, using a two-locus model, the effect of SI (frequency-dependent selection) on a locus subject to recurrent deleterious mutations causing inbreeding depression. Simulations were performed to assess the effect of population size and linkage between the two loci on the level of inbreeding depression and genetic load. We show that the sheltering of deleterious alleles linked to the S locus strengthens inbreeding depression in small populations. We discuss the implications of our results for the evolution of SI systems.