Within-species genetic diversity is thought to reflect population size, history, ecology, and ability to adapt. Using a comprehensive collection of polymorphism data sets covering approximately 3000 animal species, we show that the widely used mitochondrial DNA (mtDNA) marker does not reflect species abundance or ecology: mtDNA diversity is not higher in invertebrates than in vertebrates, in marine than in terrestrial species, or in small than in large organisms. Nuclear loci, in contrast, fit these intuitive expectations. The unexpected mitochondrial diversity distribution is explained by recurrent adaptive evolution, challenging the neutral theory of molecular evolution and questioning the relevance of mtDNA in biodiversity and conservation studies.

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.

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 clocklike 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.

Mitochondrial DNA (mtDNA) is the most popular marker of molecular diversity in animals, primarily because of its elevated mutation rate. After >20 years of intensive usage, the extent of mitochondrial evolutionary rate variations across species, their practical consequences on sequence analysis methods, and the ultimate reasons for mtDNA hypermutability are still largely unresolved issues. Using an extensive cytochrome b data set, fossil data, and taking advantage of the decoupled dynamics of synonymous and nonsynonymous substitutions, we measure the lineage-specific mitochondrial mutation rate across 1,696 mammalian species and compare it with the nuclear rate. We report an unexpected 2 orders of magnitude mitochondrial mutation rate variation between lineages: cytochrome b third codon positions are renewed every 1-2 Myr, in average, in the fastest evolving mammals, whereas it takes >100 Myr in slow-evolving lineages. This result has obvious implications in the fields of molecular phylogeny, molecular dating, and population genetics. Variations of mitochondrial substitution rate across species are partly explained by body mass, longevity, and age of female sexual maturity. The classical metabolic rate and generation time hypothesis, however, do not fully explain the observed patterns, especially a stronger effect of longevity in long-lived than in short-lived species. We propose that natural selection tends to decrease the mitochondrial mutation rate in long-lived species, in agreement with the mitochondrial theory of aging.

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Background: During the last ten years, major advances have been made in characterizing and understanding the evolution of mitochondrial DNA, the most popular marker of molecular biodiversity. Several important results were recently reported using mammals as model organisms, including (i) the absence of relationship between mitochondrial DNA diversity and life-history or ecological variables, (ii) the absence of prominent adaptive selection, contrary to what was found in invertebrates, and (iii) the unexpectedly large variation in neutral substitution rate among lineages, revealing a possible link with species maximal longevity. We propose to challenge these results thanks to the bird/mammal comparison. Direct estimates of population size are available in birds, and this group presents striking life-history trait differences with mammals (higher massspecific metabolic rate and longevity). These properties make birds the ideal model to directly test for population size effects, and to discriminate between competing hypotheses about the causes of substitution rate variation.

A fundamental challenge in population genetics and molecular evolution is to understand the forces shaping the patterns of genetic diversity within and among species. Among them, mating systems are thought to have important influences on molecular diversity and genome evolution. Selfing is expected to reduce effective population size, N e , and effective recombination rates, directly leading to reduced polymorphism and increased linkage disequilibrium compared with outcrossing. Increased isolation between populations also results directly from selfing or indirectly from evolutionary changes, such as small flowers and low pollen output, leading to greater differentiation of molecular markers than under outcrossing. The lower effective recombination rate increases the likelihood of hitch-hiking, further reducing within-deme diversity of selfers and thus increasing their genetic differentiation. There are also indirect effects on molecular evolutionary processes. Low N e reduces the efficacy of selection; in selfers, selection should thus be less efficient in removing deleterious mutations. The rarity of heterozygous sites in selfers leads to infrequent action of biased conversion towards GC, which tends to increase sequences' GC content in the most highly recombining genome regions of outcrossers. To test these predictions in plants, we used a newly developed sequence polymorphism database to investigate the effects of mating system differences on sequence polymorphism and genome evolution in a wide set of plant species. We also took into account other life-history traits, including life form (whether annual or perennial herbs, and woody perennial) and the modes of pollination and seed dispersal, which are known to affect enzyme and DNA marker polymorphism. We show that among various life-history traits, mating systems have the greatest influence on patterns of polymorphism.

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.