Daniel Ortiz-Barrientos

Divergent selection and heterogeneous genomic divergence

Levels of genetic differentiation between populations can be highly variable across the genome, with divergent selection contributing to such heterogeneous genomic divergence. For example, loci under divergent selection and those tightly physically linked to them may exhibit stronger differentiation than neutral regions with weak or no linkage to such loci. Divergent selection can also increase genome‐wide neutral differentiation by reducing gene flow (e.g. by causing ecological speciation), thus promoting divergence via the stochastic effects of genetic drift. These consequences of divergent selection are being reported in recently accumulating studies that identify: (i) ‘outlier loci’ with higher levels of divergence than expected under neutrality, and (ii) a positive association between the degree of adaptive phenotypic divergence and levels of molecular genetic differentiation across population pairs [‘isolation by adaptation’ (IBA)]. The latter pattern arises because as adaptive divergence increases, gene flow is reduced (thereby promoting drift) and genetic hitchhiking increased. Here, we review and integrate these previously disconnected concepts and literatures. We find that studies generally report 5–10% of loci to be outliers. These selected regions were often dispersed across the genome, commonly exhibited replicated divergence across different population pairs, and could sometimes be associated with specific ecological variables. IBA was not infrequently observed, even at neutral loci putatively unlinked to those under divergent selection. Overall, we conclude that divergent selection makes diverse contributions to heterogeneous genomic divergence. Nonetheless, the number, size, and distribution of genomic regions affected by selection varied substantially among studies, leading us to discuss the potential role of divergent selection in the growth of regions of differentiation (i.e. genomic islands of divergence), a topic in need of future investigation.

Strong Amerind/White sex bias and a possible sephardic contribution among the founders of a population in Northwest Colombia

Historical and genetic evidences suggest that the recently founded population of Antioquia (Colombia) is potentially useful for the genetic mapping of complex traits. This population was established in the 16th-17th centuries through the admixture of Amerinds, Europeans, and Africans and grew in relative isolation until the late 19th century. To examine the origin of the founders of Antioquia, we typed 11 markers on the nonrecombining portion of the Y chromosome and four markers on mtDNA in a sample of individuals with confirmed Antioquian ancestry. The polymorphisms on the Y chromosome (five biallelic markers and six microsatellites) allow an approximation to the origin of founder men, and those on mtDNA identify the four major founder Native American lineages. These data indicate that approximately 94% of the Y chromosomes are European, 5% are African, and 1% are Amerind. Y-chromosome data are consistent with an origin of founders predominantly in southern Spain but also suggest that a fraction came from northern Iberia and that some possibly had a Sephardic origin. In stark contrast with the Y-chromosome, approximately 90% of the mtDNA gene pool of Antioquia is Amerind, with the frequency of the four Amerind founder lineages being closest to Native Americans currently living in the area. These results indicate a highly asymmetric pattern of mating in early Antioquia, involving mostly immigrant men and local native women. The discordance of our data with blood-group estimates of admixture suggests that the number of founder men was larger than that of women.

Autosomal, mtDNA, and Y-Chromosome Diversity in Amerinds: Pre- and Post-Columbian Patterns of Gene Flow in South America

To evaluate sex-specific differences in gene flow between Native American populations from South America and between those populations and recent immigrants to the New World, we examined the genetic diversity at uni- and biparental genetic markers of five Native American populations from Colombia and in published surveys from native South Americans. The Colombian populations were typed for five polymorphisms in mtDNA, five restriction sites in the beta-globin gene cluster, the DQA1 gene, and nine autosomal microsatellites. Elsewhere, we published results for seven Y-chromosome microsatellites in the same populations. Autosomal polymorphisms showed a mean G(ST) of 6.8%, in agreement with extensive classical marker studies of South American populations. MtDNA and Y-chromosome markers resulted in G(ST) values of 0.18 and 0.165, respectively. When only Y chromosomes of confirmed Amerind origin were used in the calculations (as defined by the presence of allele T at locus DYS199), G(ST) increased to 0.22. G(ST) values calculated from published data for other South American natives were 0.3 and 0.29 for mtDNA and Amerind Y chromosomes, respectively. The concordance of these estimates does not support an important difference in migration rates between the sexes throughout the history of South Amerinds. Admixture analysis of the Colombian populations suggests an asymmetric pattern of mating involving mostly immigrant men and native women.

Recombination and the divergence of hybridizing species

The interplay between hybridization and recombination can have a dramatic effect on the likelihood of speciation or persistence of incompletely isolated species. Many models have suggested recombination can oppose speciation, and several recent empirical investigations suggest that reductions in recombination between various components of reproductive isolation and/or adaptation can allow species to persist in the presence of gene flow. In this article, we discuss these ideas in relation to speciation models, phylogenetic analyses, and species concepts. In particular, we revisit genetic architectures and population mechanisms that create genetic correlations and facilitate divergence in the face of gene flow. Linkage among genes contributing to adaptation or reproductive isolation due to chromosomal rearrangements as well as pleiotropy or proximity of loci can greatly increase the odds of species divergence or persistence. Finally, we recommend recombination to be a focus of inquiry when studying the origins of biological diversity.

The Genetics and Ecology of Reinforcement

Reinforcement, the evolution of prezygotic reproductive barriers by natural selection in response to maladaptive hybridization, is one of the most debated processes in speciation. Critics point to “fatal” conceptual flaws for sympatric evolution of prezygotic isolation, but recent theoretical and empirical work on genetics and ecology of reinforcement suggests that such criticisms can be overcome. New studies provide evidence for reinforcement in frogs, fish, insects, birds, and plants. While such evidence lays to rest the argument over reinforcements existence, our understanding remains incomplete. We lack data on (1) the genetic basis of female preferences and the links between genetics of pre‐ and postzygotic isolation, (2) the ecological basis of reproductive isolation, (3) connections between prezygotic isolation between species and within‐species sexual selection (potentially leading to a “cascade” of effects on reproductive isolation), (4) the role of habitat versus mate preference in reinforcement, and (5) additional detailed comparative studies. Here, we review data on these issues and highlight why they are important for understanding speciation.

The Genetics of Speciation by Reinforcement

Reinforcement occurs when natural selection strengthens behavioral discrimination to prevent costly interspecies matings, such as when matings produce sterile hybrids. This evolutionary process can complete speciation, thereby providing a direct link between Darwins theory of natural selection and the origin of new species. Here, by examining a case of speciation by reinforcement in Drosophila, we present the first high-resolution genetic study of variation within species for female mating discrimination that is enhanced by natural selection. We show that reinforced mating discrimination is inherited as a dominant trait, exhibits variability within species, and may be influenced by a known set of candidate genes involved in olfaction. Our results show that the genetics of reinforced mating discrimination is different from the genetics of mating discrimination between species, suggesting that overall mating discrimination might be a composite phenomenon, which in Drosophila could involve both auditory and olfactory cues. Examining the genetics of reinforcement provides a unique opportunity for both understanding the origin of new species in the face of gene flow and identifying the genetic basis of adaptive female species preferences, two major gaps in our understanding of speciation.

An association study of bipolar mood disorder (type I) with the 5-HTTLPR serotonin transporter polymorphism in a human population isolate from Colombia.

The short variant of a functional length polymorphism in the promoter region of the serotonin transporter has been associated with several behavioural and psychiatric traits, including bipolar mood disorder. The same short allele has also been implicated as a modifier of the bipolar phenotype. Here we evaluate the etiologic/modifier role of this polymorphism in a case (N=103) / control (N=112) sample for bipolar mood disorder (type I) collected from an isolated South American population. We did not detect an association between bipolar disorder and the 5-HTT promoter polymorphism in this sample. However, an excess of the short allele was seen in younger cases and in cases with psychotic symptoms. When combined with data from the literature, the increased frequency of the short allele in patients with psychotic symptoms was statistically significant.

The origins of reproductive isolation in plants

Reproductive isolation in plants occurs through multiple barriers that restrict gene flow between populations, but their origins remain uncertain. Work in the past decade has shown that postpollination barriers, such as the failure to form hybrid seeds or sterility of hybrid offspring, are often less strong than prepollination barriers. Evidence implicates multiple evolutionary forces in the origins of reproductive barriers, including mutation, stochastic processes and natural selection. Although adaptation to different environments is a common element of reproductive isolation, genomic conflicts also play a role, including female meiotic drive. The genetic basis of some reproductive barriers, particularly flower colour influencing pollinator behaviour, is well understood in some species, but the genetic changes underlying many other barriers, especially pollen-stylar interactions, are largely unknown. Postpollination barriers appear to accumulate at a faster rate in annuals compared with perennials, due in part to chromosomal rearrangements. Chromosomal changes can be important isolating barriers in themselves but may also reduce the recombination of genes contributing to isolation. Important questions for the next decade include identifying the evolutionary forces responsible for chromosomal rearrangements, determining how often prezygotic barriers arise due to selection against hybrids, and establishing the relative importance of genomic conflicts in speciation.

Gene expression divergence and the origin of hybrid dysfunctions.

Hybrids between closely related species are often sterile or inviable as a consequence of failed interactions between alleles from the different species. Most genetic studies have focused on localizing the alleles associated with these failed interactions, but the mechanistic/biochemical nature of the failed interactions is poorly understood. This review discusses recent studies that may contribute to our understanding of these failed interactions. We focus on the possible contribution of failures in gene expression as an important contributor to hybrid dysfunctions. Although regulatory pathways that share elements in highly divergent taxa may contribute to hybrid dysfunction, various studies suggest that misexpression may be disproportionately great in regulatory pathways containing rapidly evolving, particularly male-biased, genes. We describe three systems that have been analyzed recently with respect to global patterns of gene expression in hybrids versus pure species, each in Drosophila. These studies reveal that quantitative misexpression of genes is associated with hybrid dysfunction. Misexpression of genes has been documented in sterile hybrids relative to pure species, and variation in upstream factors may sometimes cause the over- or under-expression of genes resulting in hybrid sterility or inviability. Studying patterns of evolution between species in regulatory pathways, such as spermatogenesis, should help in identifying which genes are more likely to be contributors to hybrid dysfunction. Ultimately, we hope more functional genetic studies will complement our understanding of the genetic disruptions leading to hybrid dysfunctions and their role in the origin of species.

Evidence for a One-Allele Assortative Mating Locus

Theoretical models have shown that speciation with gene flow can occur readily via a “one-allele mechanism,” where the spread of the same allele within both of two diverging species reduces their subsequent hybridization. Here we present direct genetic evidence for such an allele in Drosophila pseudoobscura. Alleles conferring high or low assortative mating in D. pseudoobscura produce the same effects when inserted into D. persimilis. This observation suggests that the type of genetic variation that is most conducive to controversial modes of speciation with gene flow, such as reinforcement or sympatric speciation, is present in nature.