Chromosomal rearrangements as a major mechanism in the onset of reproductive isolation in Saccharomyces cerevisiae.
ABSTRACT: Understanding the molecular basis of how reproductive isolation evolves between individuals from the same species offers valuable insight into patterns of genetic differentiation as well as the onset of speciation [1, 2]. The yeast Saccharomyces cerevisiae constitutes an ideal model partly due to its vast ecological range, high level of genetic diversity [3-6], and laboratory-amendable sexual reproduction. Between S. cerevisiae and its sibling species in the Saccharomyces sensu stricto complex, reproductive isolation acts postzygotically and could be attributed to chromosomal rearrangements , cytonuclear incompatibility [8, 9], and antirecombination [10, 11], although the implication of these mechanisms at the incipient stage of speciation remains unclear due to further divergence in the nascent species. Recently, several studies assessed the onset of intraspecific reproductive isolation in S. cerevisiae by evaluating the effect of the mismatch repair system [12-14] or by fostering incipient speciation using the same initial genetic background [15-18]. Nevertheless, the overall genetic diversity within this species was largely overlooked, and no systematic evaluation has been performed. Here, we carried out the first species-wide survey for postzygotic reproductive isolation in S. cerevisiae. We crossed 60 natural isolates sampled from diverse niches with the reference strain S288c and identified 16 cases of reproductive isolation with reduced offspring viabilities ranging from 44% to 86%. Using different mapping strategies, we identified reciprocal translocations in a large fraction of all isolates surveyed, indicating that large-scale chromosomal rearrangements might play a major role in the onset of reproductive isolation in this species.
Project description:BACKGROUND:A key to understanding the origins of species is determining the evolutionary processes that drive the patterns of genomic divergence during speciation. New genomic technologies enable the study of high-resolution genomic patterns of divergence across natural speciation continua, where taxa pairs with different levels of reproductive isolation can be used as proxies for different stages of speciation. Empirical studies of these speciation continua can provide valuable insights into how genomes diverge during speciation. METHODS:We examine variation across a handful of genomic regions in parapatric and allopatric populations of Heliconius butterflies with varying levels of reproductive isolation. Genome sequences were mapped to 2.2-Mb of the H. erato genome, including 1-Mb across the red color pattern locus and multiple regions unlinked to color pattern variation. RESULTS:Phylogenetic analyses reveal a speciation continuum of pairs of hybridizing races and incipient species in the Heliconius erato clade. Comparisons of hybridizing pairs of divergently colored races and incipient species reveal that genomic divergence increases with ecological and reproductive isolation, not only across the locus responsible for adaptive variation in red wing coloration, but also at genomic regions unlinked to color pattern. DISCUSSION:We observe high levels of divergence between the incipient species H. erato and H. himera, suggesting that divergence may accumulate early in the speciation process. Comparisons of genomic divergence between the incipient species and allopatric races suggest that limited gene flow cannot account for the observed high levels of divergence between the incipient species. CONCLUSIONS:Our results provide a reconstruction of the speciation continuum across the H. erato clade and provide insights into the processes that drive genomic divergence during speciation, establishing the H. erato clade as a powerful framework for the study of speciation.
Project description:Although microorganisms account for the largest fraction of Earth's biodiversity, we know little about how their reproductive barriers evolve. Sexual microorganisms such as Saccharomyces yeasts rapidly develop strong intrinsic post-zygotic isolation, but the role of extrinsic isolation in the early speciation process remains to be investigated. We measured the growth of F1 hybrids between two incipient species of Saccharomyces paradoxus to assess the presence of extrinsic post-zygotic isolation across 32 environments. More than 80% of hybrids showed either partial dominance of the best parent or over-dominance for growth, revealing no fitness defects in F1 hybrids. Extrinsic reproductive isolation therefore likely plays little role in limiting gene flow between incipient yeast species and is not a requirement for speciation.
Project description:BACKGROUND AND AIMS:The events leading to speciation are best investigated in systems where speciation is ongoing or incomplete, such as incipient species. By examining reproductive barriers among incipient sister taxa and their congeners we can gain valuable insights into the relative timing and importance of the various barriers involved in the speciation process. The aim of this study was to identify the reproductive barriers among sexually deceptive orchid taxa in the genus Chiloglottis. METHODS:The study targeted four closely related taxa with varying degrees of geographic overlap. Chemical, morphological and genetic evidence was combined to explore the basis of reproductive isolation. Of primary interest was the degree of genetic differentiation among taxa at both nuclear and chloroplast DNA markers. To objectively test whether or not species boundaries are defined by the chemistry that controls pollinator specificity, genetic analysis was restricted to samples of known odour chemistry. KEY RESULTS:Floral odour chemical analysis was performed for 600+ flowers. The three sympatric taxa were defined by their specific chiloglottones, the semiochemicals responsible for pollinator attraction, and were found to be fully cross-compatible. Multivariate morphometric analysis could not reliably distinguish among the four taxa. Although varying from very low to moderate, significant levels of genetic differentiation were detected among all pairwise combinations of taxa at both nuclear and chloroplast loci. However, the levels of genetic differentiation were lower than expected for mature species. Critically, a lack of chloroplast DNA haplotype sharing among the morphologically indistinguishable and most closely related taxon pair confirmed that chemistry alone can define taxon boundaries. CONCLUSIONS:The results confirmed that pollinator isolation, mediated by specific pollinator attraction, underpins strong reproductive isolation in these taxa. A combination of large effective population sizes, initial neutral mutations in the genes controlling floral scent, and a pool of available pollinators likely drives diversity in this system.
Project description:Gene flow tends to impede the accumulation of genetic divergence. Here, we determine the limits for the evolution of postzygotic reproductive isolation in a model of two populations that are connected by gene flow. We consider two selective mechanisms for the creation and maintenance of a genetic barrier: local adaptation leads to divergence among incipient species due to selection against migrants, and Dobzhansky-Muller incompatibilities (DMIs) reinforce the genetic barrier through selection against hybrids. In particular, we are interested in the maximum strength of the barrier under a limited amount of local adaptation, a challenge that many incipient species may initially face. We first confirm that with classical two-locus DMIs, the maximum amount of local adaptation is indeed a limit to the strength of a genetic barrier. However, with three or more loci and cryptic epistasis, this limit holds no longer. In particular, we identify a minimal configuration of three epistatically interacting mutations that is sufficient to confer strong reproductive isolation. This article is part of the theme issue 'Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers'.
Project description:Mapping hybrid defects in contact zones between incipient species can identify genomic regions contributing to reproductive isolation and reveal genetic mechanisms of speciation. The house mouse features a rare combination of sophisticated genetic tools and natural hybrid zones between subspecies. Male hybrids often show reduced fertility, a common reproductive barrier between incipient species. Laboratory crosses have identified sterility loci, but each encompasses hundreds of genes. We map genetic determinants of testis weight and testis gene expression using offspring of mice captured in a hybrid zone between M. musculus musculus and M. m. domesticus. Many generations of admixture enables high-resolution mapping of loci contributing to these sterility-related phenotypes. We identify complex interactions among sterility loci, suggesting multiple, non-independent genetic incompatibilities contribute to barriers to gene flow in the hybrid zone.
Project description:Ecological speciation occurs when ecologically based, divergent selection causes the evolution of reproductive isolation. There are many empirical examples of this process; however, there exists a poorly characterized stage during which the traits that distinguish species ecologically and reproductively segregate in a single population. By using a combination of genetic mapping, mate-choice experiments, field observations, and population genetics, we studied a butterfly population with a mimetic wing color polymorphism and found that the butterflies exhibited partial, color-based, assortative mate preference. These traits represent the divergent, ecologically based signal and preference components of sexual isolation that usually distinguish incipient and sibling species. The association between behavior and recognition trait in a single population may enhance the probability of speciation and provides an example of the missing link between an interbreeding population and isolated species.
Project description:BACKGROUND:The Pleistocene climatic oscillations are considered as a major driving force of intraspecific divergence and speciation. During Ice Ages, populations isolated in allopatric glacial refugia can experience differentiation in reproductive traits through divergence in selection regimes. This phenomenon may lead to reproductive isolation and dramatically accentuates the consequences of the climatic oscillations on species. Alternatively, when reproductive isolation is incomplete and populations are expanding again, further mating between the formerly isolated populations can result in the formation of a hybrid zone, genetic introgression or reinforcement speciation through reproductive trait displacements. Therefore changes in reproductive traits driven by population movements during climatic oscillations can act as an important force in promoting pre-zygotic isolation. Notwithstanding, divergence of reproductive traits has not been approached in the context of climatic oscillations. Here we investigate the impact of population movements driven by climatic oscillations on a reproductive trait of a bumblebee species (Bombus lapidarius). We characterise the pattern of variation and differentiation across the species distribution (i) with five genes (nuclear and mitochondrial), and (ii) in the chemical composition of male marking secretions (MMS), a key trait for mate attraction in bumblebees. RESULTS:Our results provide evidence that populations have experienced a genetic allopatric differentiation, in at least three main refugia (the Balkans, Centre-Eastern Europe, and Southern Italy) during Quaternary glaciations. The comparative chemical analyses show that populations from the Southern Italian refugium have experienced MMS differentiation and an incipient speciation process from another refugium. The meeting of Southern Italian populations with other populations as a result of range expansion at a secondary contact zone seems to have led to a reinforcement process on local MMS patterns. CONCLUSIONS:This study suggests that population movement during Quaternary climatic oscillations can lead to divergence in reproductive traits by allopatric differentiation during Ice Ages and by reinforcement during post-glacial recolonization.
Project description:Disruptive selection of life-cycle timing may cause temporal isolation directly and, ultimately, allochronic speciation. Despite the fact that segregation of the reproductive period among related species has been broadly observed across taxa, it remains controversial whether temporal isolation can function as the primary process of speciation. In the Japanese winter geometrid moth Inurois punctigera, allochronic divergence has resulted from climatic disruption of the reproductive period. In habitats with severe midwinter, two sympatric groups of moth reproduce allochronically in early and late winter. These groups are genetically diverging sister lineages and now co-occur allochronically throughout Japan. By contrast, in habitats with milder midwinter these lineages form a continuous adult period and gene flow has been facilitated between the lineages. These results, together with the fact that there is no difference in larval host use, indicate that temporal isolation has been the sole mechanism for allochronic isolation in colder habitats and that allochrony is not a by-product of other adaptations. Thus, the allochronic divergence of sympatric I. punctigera populations represents an incipient speciation process driven by midwinter disruption of the reproductive period.
Project description:Hybridization between incipient species is expected to become progressively limited as their genetic divergence increases and reproductive isolation proceeds. Amphibian radiations and their secondary contact zones are useful models to infer the timeframes of speciation, but empirical data from natural systems remains extremely scarce. Here we follow this approach in the European radiation of tree frogs (Hyla arborea group). We investigated a natural hybrid zone between two lineages (Hyla arborea and Hyla orientalis) of Mio-Pliocene divergence (~5 My) for comparison with other hybrid systems from this group.We found concordant geographic distributions of nuclear and mitochondrial gene pools, and replicated narrow transitions (~30 km) across two independent transects, indicating an advanced state of reproductive isolation and potential local barriers to dispersal. This result parallels the situation between H. arborea and H. intermedia, which share the same amount of divergence with H. orientalis. In contrast, younger lineages show much stronger admixture at secondary contacts.Our findings corroborate the negative relationship between hybridizability and divergence time in European tree frogs, where 5 My are necessary to achieve almost complete reproductive isolation. Speciation seems to progress homogeneously in this radiation, and might thus be driven by gradual genome-wide changes rather than single speciation genes. However, the timescale differs greatly from that of other well-studied amphibians. General assumptions on the time necessary for speciation based on evidence from unrelated taxa may thus be unreliable. In contrast, comparative hybrid zone analyses within single radiations such as our case study are useful to appreciate the advance of speciation in space and time.
Project description:Speciation genes are responsible for reproductive isolation between species. By directly participating in the process of speciation, the genealogies of isolating loci have been thought to more faithfully represent species trees. The unique properties of speciation genes may provide valuable evolutionary insights and help determine the true history of species divergence. Here, we formally analyze whether genealogies from loci participating in Dobzhansky-Muller (DM) incompatibilities are more likely to be concordant with the species tree under incomplete lineage sorting (ILS). Individual loci differ stochastically from the true history of divergence with a predictable frequency due to ILS, and these expectations-combined with the DM model of intrinsic reproductive isolation from epistatic interactions-can be used to examine the probability of concordance at isolating loci. Contrary to existing verbal models, we find that reproductively isolating loci that follow the DM model are often more likely to have discordant gene trees. These results are dependent on the pattern of isolation observed between three species, the time between speciation events, and the time since the last speciation event. Results supporting a higher probability of discordance are found for both derived-derived and derived-ancestral DM pairs, and regardless of whether incompatibilities are allowed or prohibited from segregating in the same population. Our overall results suggest that DM loci are unlikely to be especially useful for reconstructing species relationships, even in the presence of gene flow between incipient species, and may in fact be positively misleading.