What can patterns of differentiation across plant genomes tell us about adaptation and speciation?

Genome scans have become a common approach to identify genomic signatures of natural selection and reproductive isolation, as well as the genomic bases of ecologically relevant phenotypes, based on patterns of polymorphism and differentiation among populations or species. Here, we review the results of studies taking genome scan approaches in plants, consider the patterns of genomic differentiation documented and their possible causes, discuss the results in light of recent models of genomic differentiation during divergent adaptation and speciation, and consider assumptions and caveats in their interpretation. We find that genomic regions of high divergence generally appear quite small in comparisons of both closely and more distantly related populations, and for the most part, these differentiated regions are spread throughout the genome rather than strongly clustered. Thus, the genome scan approach appears well-suited for identifying genomic regions or even candidate genes that underlie adaptive divergence and/or reproductive barriers. We consider other methodologies that may be used in conjunction with genome scan approaches, and suggest further developments that would be valuable. These include broader use of sequence-based markers of known genomic location, greater attention to sampling strategies to make use of parallel environmental or phenotypic transitions, more integration with approaches such as quantitative trait loci mapping and measures of gene flow across the genome, and additional theoretical and simulation work on processes related to divergent adaptation and speciation.     

Inferring the history of speciation in house mice from autosomal,X‐linked,Y‐linked and mitochondrial genes

Patterns of genetic differentiation among taxa at early stages of divergence provide an opportunity to make inferences about the history of speciation. Here, we conduct a survey of DNA‐sequence polymorphism and divergence at loci on the autosomes, X chromosome, Y chromosome and mitochondrial DNA in samples of Mus domesticus, M. musculus and M. castaneus. We analyzed our data under a divergence with gene flow model and estimate that the effective population size of M. castaneus is 200 000–400 000, of M. domesticus is 100 000–200 000 and of M. musculus is 60 000–120 000. These data also suggest that these species started to diverge approximately 500 000 years ago. Consistent with this recent divergence, we observed considerable variation in the genealogical patterns among loci. For some loci, all alleles within each species formed a monophyletic group, while at other loci, species were intermingled on the phylogeny of alleles. This intermingling probably reflects both incomplete lineage sorting and gene flow after divergence. Likelihood ratio tests rejected a strict allopatric model with no gene flow in comparisons between each pair of species. Gene flow was asymmetric: no gene flow was detected into M. domesticus, while significant gene flow was detected into both M. castaneus and M. musculus. Finally, most of the gene flow occurred at autosomal loci, resulting in a significantly higher ratio of fixed differences to polymorphisms at the X and Y chromosomes relative to autosomes in some comparisons, or just the X chromosome in others, emphasizing the important role of the sex chromosomes in general and the X chromosome in particular in speciation.     

Recombination rate variation in closely related species

Despite their importance to successful meiosis and various evolutionary processes, meiotic recombination rates sometimes vary within species or between closely related species. For example, humans and chimpanzees share virtually no recombination hotspot locations in the surveyed portion of the genomes. However, conservation of recombination rates between closely related species has also been documented, raising an apparent contradiction. Here, we evaluate how and why conflicting patterns of recombination rate conservation and divergence may be observed, with particular emphasis on features that affect recombination, and the scale and method with which recombination is surveyed. Additionally, we review recent studies identifying features influencing fine-scale and broad-scale recombination patterns and informing how quickly recombination rates evolve, how changes in recombination impact selection and evolution in natural populations, and more broadly, which forces influence genome evolution.     

The pattern of linkage disequilibrium in German Holstein cattle

This study presents a second generation of linkage disequilibrium (LD) map statistics for the whole genome of the Holstein–Friesian population, which has a four times higher resolution compared with that of the maps available so far. We used DNA samples of 810 German Holstein–Friesian cattle genotyped by the Illumina Bovine SNP50K BeadChip to analyse LD structure. A panel of 40 854 (75.6%) markers was included in the final analysis. The pairwise r² statistic of SNPs up to 5 Mb apart across the genome was estimated. A mean value of r² = 0.30 ± 0.32 was observed in pairwise distances of <25 kb and it dropped to 0.20 ± 0.24 at 50–75 kb, which is nearly the average inter‐marker space in this study. The proportion of SNPs in useful LD (r² ≥ 0.25) was 26% for the distance of 50 and 75 kb between SNPs. We found a lower level of LD for SNP pairs at the distance ≤100 kb than previously thought. Analysis revealed 712 haplo‐blocks spanning 4.7% of the genome and containing 8.0% of all SNPs. Mean and median block length were estimated as 164 ± 117 kb and 144 kb respectively. Allele frequencies of the SNPs have a considerable and systematic impact on the estimate of r². It is shown that minimizing the allele frequency difference between SNPs reduces the influence of frequency on r² estimates. Analysis of past effective population size based on the direct estimates of recombination rates from SNP data showed a decline in effective population size to N_e = 103 up to ～4 generations ago. Systematic effects of marker density and effective population size on observed LD and haplotype structure are discussed.     

Effective population size and the rate and pattern of nucleotide substitutions

Both the overall rate of nucleotide substitution and the relative proportions of synonymous and non-synonymous substitutions are predicted to vary between species that differ in effective population size (N_e). Our understanding of the genetic processes underlying these lineage-specific differences in molecular evolution is still developing. Empirical analyses indicate that variation in substitution rates and patterns caused by differences in N_e is often substantial, however, and must be accounted for in analyses of molecular evolution.     

Large global effective population sizes in Paramecium

The genetic effective population size (N(e)) of a species is an important parameter for understanding evolutionary dynamics because it mediates the relative effects of selection. However, because most N(e) estimates for unicellular organisms are derived either from taxa with poorly understood species boundaries or from host-restricted pathogens and most unicellular species have prominent phases of clonal propagation potentially subject to strong selective sweeps, the hypothesis that N(e) is elevated in single-celled organisms remains controversial. Drawing from observations on well-defined species within the genus Paramecium, we report exceptionally high levels of silent-site polymorphism, which appear to be a reflection of large N(e).     

Random genetic drift during cyclical ameiotic parthenogenesis

The classical models of population genetics assume sexual reproduction and do not apply to organisms in which parthenogenetic reproduction is alternated with sexual recombination. Under cyclic parthenogenesis, variation in rates or frequencies of parthenogenetic reproduction among clones produces selection that is independent of processes occurring in the sexual phases.In this paper I examine how selection during cyclic parthenogenesis influences random genetic drift and leads to a loss of variance among clones. To illustrate these effects, computer simulations are presented demonstrating the response of effective clone number and equilibrium clone diversity to selection and mutation.     

Triangulating the genetic basis of adaptation to multifarious selection

Understanding how natural populations adapt to their local environments is a major research theme for ecological genomics. This endeavour begins by sleuthing for shared genetic similarities among unrelated natural populations sharing adaptive traits to documented selective pressures. When the selective pressures have low dimensionality, and the genetic response is localized to a few genes of major effect, this detective work is relatively straightforward. However, in the real world, populations face a complex mixture of selective pressures and many adaptive responses are the result of changes in quantitative traits that have a polygenic genetic basis. This complex relationship between environment and adaptation presents a significant challenge. How can we begin to identify drivers of adaptation in natural settings? In this issue of Molecular Ecology, Orsini et al. (2012) take advantage of the biological attributes of the freshwater microcrustacean Daphnia ( Fig. 1 ) to disentangle multidimensional selection’s signature on the genome of populations that have repeatedly evolved adaptive responses to isolated selective pressures including predation, parasitism and anthropogenic changes in land use. Orsini et al. (2012) leverage a powerful combination of spatially structured populations in a geographic mosaic of environmental stressors, the historical archive of past genotypes preserved in lake‐bottom sediments and selection experiments to identify sets of candidate genomic regions associated with adaptation in response to these three environmental stressors. This study provides a template for future investigation in ecological genomics, combining multiple experimental approaches with the genomic investigation of a well‐studied ecological model species.

Figure 1 Open in figure viewer PowerPoint Adult Daphnia magna carrying a resting egg in the brood pouch. The water flea Daphnia is a renowned ecological model system and rapidly developing as an ecological and environmental genomics model species. Photo credit Joachim Mergeay.     

Parallel evolution? Microsatellite variation of recently isolated marine and freshwater three-spined stickleback

Variation at nine microsatellite loci, four of which are linked to phenotypic traits (spine length and lateral plate morphology) in Canadian three-spined stickleback Gasterosteus aculeatus , are used to test for selection on marine and freshwater three-spined stickleback morphs in Iceland. There are indications of strong selection on loci linked to dorsal spine length, providing another potential example of parallel divergence at the genomic level in three-spined stickleback.