Ecological speciation promoted by divergent regulation of functional genes within African cichlid fishes

Rapid ecological speciation along depth gradients has taken place independently and repeatedly in freshwater fishes. While the extent of genomic divergence between ecomorphs is often well understood, the molecular mechanisms facilitating such rapid diversification are typically unclear. In Lake Masoko, an East African crater lake, the cichlid Astatotilapia calliptera has diverged into shallow littoral and deep benthic ecomorphs with strikingly different jaw structures within the last 1,000 years. Using genome-wide transcriptome data from jaw tissue, we explore two major regulatory transcriptional mechanisms, expression and splicing QTL variants and examine their contribution to differential gene expression underpinning functional phenotypes. We identified 7,550 genes with significant differential expression between ecomorphs, of which 4.2% were regulated by cis-regulatory expression QTLs, and 6.4% were regulated by cis-regulatory splicing QTLs. There were also strong signals of divergent selection of differentially expressed genes that showed divergent regulation from expression, splicing or both QTL variants, including genes associated with major jaw plasticity and adaptation networks, adaptive immune system response, and oxidoreductase processes. These results suggest that transcriptome plasticity and modification have important roles during early-stage ecological speciation and demonstrate the role of regulatory-variants as important targets of selection driving ecologically-relevant divergence in gene expression that is associated with adaptive diversification.

Phylogeography of an Amazonian Cichlid supports strong structuration by water current and past evolution by vicariance associated to the Amazon's formation.

Amazonia is characterized by very heterogeneous riverscapes dominated by two drastically divergent water types: black (ion-poor, dissolved organic carbonate rich and acidic) and white (nutrient rich and turbid) waters. Recent phylogeographic and genomic studies have associated the ecotone formed by these environments to ecologically driven speciation in fish species. With the objective of better understanding the evolutionary forces behind the Amazonian Teleostean diversification, we sampled 240 Mesonauta festivus from 12 sites on a wide area of the Amazonian basin. These sites included three confluences of black and white water environments to seek for repeated evidences of ecological speciation at these ecotones. Our genetic dataset of 41,268 SNPs is contrasting with previous results and supports a low structuring power of water types. Conversely, we detected a strong pattern of isolation by unidirectional downstream water current and evidence of past events of vicariance potentially linked to the Amazon River formation and salt-water incursions that occurred 2.5 Mya. Using a combination of population genetic, phylogeographic analysis and environmental association models, we decomposed the spatial variance from the environmental genetic variance specifically to assess which evolutive forces have shaped inter-population differences in M. festivus’ genome. Our sampling design comprising four major Amazonian rivers and three confluences of black and white water rivers supports the possibility that past studies potentially confounded ecological speciation with a site effect unrepresentative of the full Amazonian watershed. While ecological speciation admittedly played a role in Amazonian fish species diversification, we argue that neutral evolutionary processes explain most of the divergence between M. festivus populations.

Pre- and post-mating reproductive isolation evolve independently during rapid adaptation to high temperature

Ambient temperature is one major ecological factor driving adaptation in natural populations, but its impact on the emergence of new species is not yet clear. Here, we explored the evolution of reproductive isolation during temperature adaptation by exposing 10 replicate Drosophila simulans populations to a hot temperature regime. Within less than 200 generations, both pre- and post-mating reproductive isolation evolved. The altered lipid metabolism of evolved flies also affected the cuticular hydrocarbon (CHCs) profiles. Different CHC profiles could explain the emerged assortative mating between ancestral and evolved populations. Hence, we identified the hallmark of ecological speciation driven by temperature adaptation. While this pre-mating isolation occurred only between ancestral and evolved replicate populations, post-mating reproductive isolation was observed among evolved replicate populations. We propose that epistatic interactions of reproduction-related genes between males and females resulted in adaptive co-evolution. Incompatibilities between different gene combinations favored in each replicate could explain the observed post-mating reproductive isolation. We anticipate that this mutation-order-like speciation from standing genetic variation, a new speciation process, is widespread in nature when highly polygenic traits are involved in adaptation.

Varying Intensities of Introgression Obscure Incipient Venom-Associated Speciation in the Timber Rattlesnake (Crotalus horridus)

Ecologically divergent selection can lead to the evolution of reproductive isolation through the process of ecological speciation, but the balance of responsible evolutionary forces is often obscured by an inadequate assessment of demographic history and the genetics of traits under selection. Snake venoms have emerged as a system for studying the genetic basis of adaptation because of their genetic tractability and contributions to fitness, and speciation in venomous snakes can be associated with ecological diversification such as dietary shifts and corresponding venom changes. Here, we explored the neurotoxic (type A)–hemotoxic (type B) venom dichotomy and the potential for ecological speciation among Timber Rattlesnake (Crotalus horridus) populations. Previous work identified the genetic basis of this phenotypic difference, enabling us to characterize the roles geography, history, ecology, selection, and chance play in determining when and why new species emerge or are absorbed. We identified significant genetic, proteomic, morphological, and ecological/environmental differences at smaller spatial scales, suggestive of incipient ecological speciation between type A and type B C. horridus. Range-wide analyses, however, rejected the reciprocal monophyly of venom type, indicative of varying intensities of introgression and a lack of reproductive isolation across the range. Given that we have now established the phenotypic distributions and ecological niche models of type A and B populations, genome-wide data are needed and capable of determining whether type A and type B C. horridus represent distinct, reproductively isolated lineages due to incipient ecological speciation or differentiated populations within a single species.

Connecting neuromodulation, brain development, and life history timing associated with ecological speciation in Rhagoletis pomonella

Host shifts are considered a key generator of insect biodiversity, yet how insects synchronize life history timing and preference for new hosts is not well understood. Neurochemicals such as biogenic amines play key roles in both development and behavior, and therefore provide a potential source for such synchronization. Here, we correlated life history timing, brain development, and corresponding levels of 14 neurochemicals in Rhagoletis pomonella (Diptera: Tephritidae), a species undergoing ecological speciation through an ongoing host shift from hawthorn to apple fruit. We found that adult brain differentiation in both host races was initiated only after pupal diapause ended, and at this stage the titers of precursors for several neurotransmitter pathways also increased significantly. Conversely, neurotransmitter product titres generally increased at later stages up to adult fly sexual maturation. Further analysis showed that the apple host race exhibited adult brain differentiation three weeks earlier than the hawthorn host race, which correlated with significantly lower titers of several neurochemicals, particularly biogenic amines, in the earlier developing apple race as compared to the hawthorn race. We thus propose that these neurotransmitter levels could influence the differences in life history timing and host preference observed in these two races, promoting their ongoing speciation.

Chromosomal rearrangements preserve adaptive divergence in ecological speciation

Despite increasing empirical evidence that chromosomal rearrangements may play an important role in adaptive divergence and speciation, the degree to which divergent genomic regions are associated with chromosomal rearrangements remains unclear. In this study, we provide the first whole-genome analyses of ecological speciation and chromosomal evolution in a Daphnia species complex, using chromosome-scale assemblies and natural-population sequencing of the recently diverged species pair, Daphnia pulicaria and Daphnia pulex, which occupy distinct yet overlapping habitats in North America, and the outgroup species Daphnia obtusa. Our results describe a mixed mode of geographic divergence (isolation with secondary contact) resulting in a heterogeneous landscape of genomic divergence. Large contiguous continents of divergence encompass over one third of the genome (36%) and contain nearly all the fixed differences (94%) between the species, while the background genome has been homogenized. Chromosomal rearrangements between species, including inversions and intrachromosomal translocations, are associated with the continents of divergence and capture multiple adaptive alleles in genes and pathways thought to contribute to the species phenotypic differences.

Mapping of quantitative trait loci underlying a magic trait in ongoing ecological speciation

Background Telmatochromis temporalis is a cichlid fish endemic to Lake Tanganyika. The normal and dwarf morphs of this fish are a clear example of ongoing ecological speciation, and body size plays an important role in this speciation event as a magic trait. However, the genetic basis underlying this trait has not been studied. Results Based on double-digested restriction-site associated DNA (ddRAD) sequencing of a hybrid cross between the morphs that includes F0 male, F0 female, and 206 F2 individuals, we obtained a linkage map consisting of 708 ddRAD markers in 22 linkage groups, which corresponded to the previously reported Oreochromis niloticus chromosomes, and identified one significant and five suggestive quantitative trait loci (QTL) for body size. From the body-size distribution pattern, the significant and three of the five suggestive QTL are possibly associated with genes responsible for the difference in body size between the morphs. Conclusions The QTL analysis presented here suggests that multiple genes, rather than a single gene, control morph-specific body size. The present results provide further insights about the genes underlying the morph specific body size and evolution of the magic trait during ecological speciation.

Population genetic structure of a major reef-building coral species Acropora downingi in northeastern Arabian Peninsula

Current seawater temperatures around the northeastern Arabian Peninsula resemble future global forecasts as temperatures > 35 °C are commonly observed in summer. To provide a more fundamental aim of understanding the structure of wild populations in extreme environmental conditions, we conducted a population genetic study of a widespread, regional endemic table coral species, Acropora downingi, across the northeastern Arabian Peninsula. A total of 63 samples were collected in the southern Arabian/Persian Gulf (Abu Dhabi and Qatar) and the Sea of Oman (northeastern Oman). Using RAD-seq techniques, we described the population structure of A. downingi across the study area. Pairwise G’st and distance-based analyses using neutral markers displayed two distinct genetic clusters: one represented by Arabian/Persian Gulf individuals, and the other by Sea of Oman individuals. Nevertheless, a model-based method applied to the genetic data suggested a panmictic population encompassing both seas. Hypotheses to explain the distinctiveness of phylogeographic subregions in the northeastern Arabian Peninsula rely on either (1) bottleneck events due to successive mass coral bleaching, (2) recent founder effect, (3) ecological speciation due to the large spatial gradients in physical conditions, or (4) the combination of seascape features, ocean circulation and larval traits. Neutral markers indicated a slightly structured population of A. downingi, which exclude the ecological speciation hypothesis. Future studies across a broader range of organisms are required to furnish evidence for existing hypotheses explaining a population structure observed in the study area. Though this is the most thermally tolerant acroporid species worldwide, A. downingi corals in the Arabian/Persian Gulf have undergone major mortality events over the past three decades. Therefore, the present genetic study has important implications for understanding patterns and processes of differentiation in this group, whose populations may be pushed to extinction as the Arabian/Persian Gulf warms.