An official website of the United States government
The history of riverine fish diversification is largely a product of geographic isolation. Physical barriers that reduce or eliminate gene flow between populations facilitate divergence via genetic drift and natural selection, eventually leading to speciation. For freshwater organisms, diversification is often the product of drainage basin rearrangements. In young clades where the history of isolation is the most recent, evolutionary relationships can resemble a tangled web. One especially recalcitrant group of freshwater fishes is the Johnny Darter (Etheostoma nigrum) species complex, where traditional taxonomy and molecular phylogenetics indicate a history of gene flow and conflicting inferences of species diversity. Here we assemble a genomic dataset using double digest restriction site associated DNA (ddRAD) sequencing and use phylogenomic and population genetic approaches to investigate the evolutionary history of the complex of species that includes E. nigrum, E. olmstedi, E. perlongum, and E. susanae. We reveal and validate several evolutionary lineages that we delimit as species, highlighting the need for additional work to formally describe the diversity of the Etheostoma nigrum complex. Our analyses also identify gene flow among recently diverged lineages, including one instance involving E. susanae, a localized and endangered species. Phylogeographic structure within the Etheostoma nigrum species complex coincides with major geologic events, such as parallel divergence in river basins during Pliocene inundation of the Atlantic coastal plain and multiple northward post-glacial colonization routes tracking river basin rearrangements. Our study serves as a nuanced example of how low dispersal rates coupled with geographic isolation among disconnected river systems in eastern North America has produced one of the world’s freshwater biodiversity hotspots.
more »
« less
Riverscape genomics of cichlid fishes in the lower Congo: Uncovering mechanisms of diversification in an extreme hydrological regime
Freshwater fishes are notably diverse, given that freshwater habitat represents a tiny fraction of the earth's surface, but the mechanisms generating this diversity remain poorly understood. Rivers provide excellent models to understand how freshwater diversity is generated and maintained across heterogeneous habitats. In particular, the lower Congo River (LCR) consists of a dynamic hydroscape exhibiting extraordinary aquatic biodiversity, endemicity, morphological and ecological specialization. Previous studies have suggested that the numerous high-energy rapids throughout the LCR form physical barriers to gene flow, thus facilitating diversification and speciation, generating ichthyofaunal diversity. However, this hypothesis has not been fully explored using genome-wide SNPs for fish species distributed across the LCR. Here, we examined four lamprologine cichlids endemic to the LCR that are distributed along the river without range overlap. Using genome-wide SNP data, we tested the hypotheses that high-energy rapids serve as physical barriers to gene flow that generate genetic divergence at interspecific and intraspecific levels, and that gene flow occurs primarily in a downstream direction. Our results are consistent with the prediction that powerful rapids sometimes act as a barrier to gene flow but also suggest that, at certain temporal and spatial scales, they may provide multidirectional dispersal opportunities for riverine rheophilic cichlid fishes. These results highlight the complexity of diversification processes in rivers and the importance of assessing such processes across different riverscapes.
more »
« less
- Award ID(s):
- 1655227
- PAR ID:
- 10327577
- Date Published:
- Journal Name:
- Molecular ecology
- ISSN:
- 0962-1083
- Page Range / eLocation ID:
- 1-17
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Chen, Tzong-Yueh (Ed.)Salinity gradients act as strong environmental barriers that limit the distribution of aquatic organisms. Changes in gene expression associated with transitions between freshwater and saltwater environments can provide insights into organismal responses to variation in salinity. We used RNA-sequencing (RNA-seq) to investigate genome-wide variation in gene expression between a hypersaline population and a freshwater population of the livebearing fish speciesLimia perugiae(Poeciliidae). Our analyses of gill gene expression revealed potential molecular mechanisms underlying salinity tolerance in this species, including the enrichment of genes involved in ion transport, maintenance of chemical homeostasis, and cell signaling in the hypersaline population. We also found differences in gene expression patterns associated with cell-cycle and protein-folding processes between the hypersaline and freshwaterL.perugiae. Bidirectional freshwater-saltwater transitions have occurred repeatedly during the diversification of fishes, allowing for broad-scale examination of repeatable patterns in evolution. Therefore, we compared transcriptomic variation inL.perugiaewith other teleosts that have made freshwater-saltwater transitions to test for convergence in gene expression. Among the four distantly related population pairs from high- and low-salinity environments that we included in our analysis, we found only ten shared differentially expressed genes, indicating little evidence for convergence. However, we found that differentially expressed genes shared among three or more lineages were functionally enriched for ion transport and immune functioning. Overall, our results—in conjunction with other recent studies—suggest that different genes are involved in salinity transitions across disparate lineages of teleost fishes.more » « less
-
Hancock, Angela (Ed.)Abstract Geographic barriers are frequently invoked to explain genetic structuring across the landscape. However, inferences on the spatial and temporal origins of population variation have been largely limited to evolutionary neutral models, ignoring the potential role of natural selection and intrinsic genomic processes known as genomic architecture in producing heterogeneity in differentiation across the genome. To test how variation in genomic characteristics (e.g. recombination rate) impacts our ability to reconstruct general patterns of differentiation between species that cooccur across geographic barriers, we sequenced the whole genomes of multiple bird populations that are distributed across rivers in southeastern Amazonia. We found that phylogenetic relationships within species and demographic parameters varied across the genome in predictable ways. Genetic diversity was positively associated with recombination rate and negatively associated with species tree support. Gene flow was less pervasive in genomic regions of low recombination, making these windows more likely to retain patterns of population structuring that matched the species tree. We further found that approximately a third of the genome showed evidence of selective sweeps and linked selection, skewing genome-wide estimates of effective population sizes and gene flow between populations toward lower values. In sum, we showed that the effects of intrinsic genomic characteristics and selection can be disentangled from neutral processes to elucidate spatial patterns of population differentiation.more » « less
-
Abstract Can knowledge about genome architecture inform biogeographic and phylogenetic inference? Selection, drift, recombination, and gene flow interact to produce a genomic landscape of divergence wherein patterns of differentiation and genealogy vary nonrandomly across the genomes of diverging populations. For instance, genealogical patterns that arise due to gene flow should be more likely to occur on smaller chromosomes, which experience high recombination, whereas those tracking histories of geographic isolation (reduced gene flow caused by a barrier) and divergence should be more likely to occur on larger and sex chromosomes. In Amazonia, populations of many bird species diverge and introgress across rivers, resulting in reticulated genomic signals. Herein, we used reduced representation genomic data to disentangle the evolutionary history of 4 populations of an Amazonian antbird, Thamnophilus aethiops, whose biogeographic history was associated with the dynamic evolution of the Madeira River Basin. Specifically, we evaluate whether a large river capture event ca. 200 Ka, gave rise to reticulated genealogies in the genome by making spatially explicit predictions about isolation and gene flow based on knowledge about genomic processes. We first estimated chromosome-level phylogenies and recovered 2 primary topologies across the genome. The first topology (T1) was most consistent with predictions about population divergence and was recovered for the Z-chromosome. The second (T2), was consistent with predictions about gene flow upon secondary contact. To evaluate support for these topologies, we trained a convolutional neural network to classify our data into alternative diversification models and estimate demographic parameters. The best-fit model was concordant with T1 and included gene flow between non-sister taxa. Finally, we modeled levels of divergence and introgression as functions of chromosome length and found that smaller chromosomes experienced higher gene flow. Given that (1) genetrees supporting T2 were more likely to occur on smaller chromosomes and (2) we found lower levels of introgression on larger chromosomes (and especially the Z-chromosome), we argue that T1 represents the history of population divergence across rivers and T2 the history of secondary contact due to barrier loss. Our results suggest that a significant portion of genomic heterogeneity arises due to extrinsic biogeographic processes such as river capture interacting with intrinsic processes associated with genome architecture. Future phylogeographic studies would benefit from accounting for genomic processes, as different parts of the genome reveal contrasting, albeit complementary histories, all of which are relevant for disentangling the intricate geogenomic mechanisms of biotic diversification. [Amazonia; biogeography; demographic modeling; gene flow; gene tree; genome architecture; geogenomics; introgression; linked selection; neural network; phylogenomic; phylogeography; reproductive isolation; speciation; species tree.]more » « less
-
Abstract Rivers are prominent landscape features, acting as key promoters of diversification among freshwater organisms. Albeit generally considered potential barriers to species movement, they may also facilitate gene flow and structure populations of semiaquatic species (Riverine Thruway Hypothesis, RTH). We evaluated the role of rivers on the processes responsible for current genetic variation in the semiaquatic frog Pseudis bolbodactyla, testing whether each hydrographic basin harbours distinct genetic lineages. We sequenced three markers on 166 samples from 13 localities along the Paraná (PR), Araguaia–Tocantins (AT), and São Francisco (SF) River basins in Brazil. We recovered three populations geographically matching each hydrographic basin. Our results indicate migration among basins, with the best model selected using approximate Bayesian computation, including migration between AT and SF and ancient gene flow from PR to the AT–SF ancestor. Our findings are likely related to the orogenic events in Central Brazil dating to the Late Miocene (5 Mya), when hydrographic basins and the geomorphological features of the Brazilian Shield were formed. This suggests that P. bolbodactyla probably represents a species complex, with each lineage occurring in a distinct hydrographic basin, matching the predictions of the RTH.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/DOI: 10.1111/mec.16495
