skip to main content


Title: 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
NSF-PAR ID:
10327577
Author(s) / Creator(s):
; ; ; ; ;
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
  1. 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
  2. Abstract

    Assessments of spatial and temporal congruency across taxa from genetic data provide insights into the extent to which similar processes structure communities. However, for coastal regions that are affected continuously by cyclical sea‐level changes over the Pleistocene, congruent interspecific response will not only depend upon codistributions, but also on similar dispersal histories among taxa. Here, we use SNPs to test for concordant genetic structure among four codistributed taxa of freshwater fishes (Teleostei: Characidae) along the Brazilian Atlantic coastal drainages. Based on population relationships and hierarchical genetic structure analyses, we identify all taxa share the same geographic structure suggesting the fish utilized common passages in the past to move between river basins. In contrast to this strong spatial concordance, model‐based estimates of divergence times indicate that despite common routes for dispersal, these passages were traversed by each of the taxa at different times resulting in varying degrees of genetic differentiation across barriers with most divergences dating to the Upper Pleistocene, even when accounting for divergence with gene flow. Interestingly, when this temporal dissonance is viewed through the lens of the species‐specific ecologies, it suggests that an ecological sieve influenced whether species dispersed readily, with an ecological generalist showing the highest propensity for historical dispersal among the isolated rivers of the Brazilian coast (i.e., the most recent divergence times and frequent gene flow estimated for barriers). We discuss how our findings, and in particular what the temporal dissonance, despite common geographic passages, suggest about past dispersal structuring coastal communities as a function of ecological and paleo‐landscape sieves.

     
    more » « less
  3. Abstract Aim

    To investigate how putative barriers, forest refugia, and ecological gradients across the lower Guineo‐Congolian rain forest shape genetic and phenotypic divergence in the leaf‐folding frogAfrixalus paradorsalis, and examine the role of adjacent land bridge and sky‐islands in diversification.

    Location

    The Lower Guineo‐Congolian Forest, the Cameroonian Volcanic Line (CVL), and Bioko Island, Central Africa.

    Taxon

    Afrixalus paradorsalis(Family: Hyperoliidae), an African leaf‐folding frog.

    Methods

    We used molecular and phenotypic data to investigate diversity and divergence among theA. paradorsalisspecies complex distributed across lowland rain forests, a land bridge island, and mountains in Central Africa. We examined the coincidence of population boundaries, landscape features, divergence times, and spatial patterns of connectivity and diversity, and subsequently performed demographic modelling using genome‐wide SNP variation to distinguish among divergence mechanisms in mainland (riverine barriers, forest refugia, ecological gradients) and land bridge island populations (vicariance, overwater dispersal).

    Results

    We detected four genetically distinct allopatric populations corresponding to Bioko Island, the CVL, and two lowland rain forest populations split by the Sanaga River. Although lowland populations are phenotypically indistinguishable, pronounced body size evolution occurs at high elevation, and the timing of the formation of the high elevation population coincides with mountain uplift in the CVL. Spatial analyses and demographic modelling revealed population divergence across mainland Lower Guinea is best explained by forest refugia rather than riverine barriers or ecological gradients, and that the Bioko Island population divergence is best explained by vicariance (marine incursion) rather than overseas dispersal.

    Main conclusions

    We provide growing support for the important role of forest refugia in driving intraspecific divergences in the Guineo‐Congolian rain forest. InA. paradorsalis, sky‐islands in the CVL have resulted in greater genetic and phenotypic divergences than marine incursions of the land bridge Bioko Island, highlighting important differences in patterns of island‐driven diversification in Lower Guinea.

     
    more » « less
  4. 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
  5. Abstract Aim

    To test the importance of alternative diversification drivers and biogeographical processes for the evolution of Amazonian upland forest birds through a densely sampled analysis of diversification of the endemic Amazonian genusRhegmatorhinaat multiple taxonomic and temporal scales.

    Location

    Amazonia.

    Taxon

    Antbirds (Thamnophilidae).

    Methods

    We sequenced four mtDNAand nuclear gene regions of 120 individuals from 50 localities representing all recognized species and subspecies of the genus. We performed molecular phylogenetic analyses using both gene tree and species tree methods, molecular dating analysis and estimated population demographic history and gene flow.

    Results

    Dense sampling throughout the distribution ofRhegmatorhinarevealed that the main Amazonian rivers delimit the geographic distribution of taxa as inferred from mtDNAlineages. Molecular phylogenetic analyses resulted in a strongly supported phylogenetic hypothesis for the genus, with two main clades currently separated by the Madeira River. Molecular dating analysis indicated diversification during the Quaternary. Reconstruction of recent demographic history of populations revealed a trend for population expansion in eastern Amazonia and stability in the west. Estimates of gene flow corroborate the possibility that migration after divergence had some influence on the current patterns of diversity.

    Main Conclusions

    Based on broad‐scale sampling, a clarification of taxonomic boundaries, and strongly supported phylogenetic relationships, we confirm that, first, mitochondrial lineages within this upland forest Amazonian bird genus agree with spatial patterns known for decades based on phenotypes, and second, that most lineages are geographically delimited by the large Amazonian rivers. The association between past demographic changes related to palaeoclimatic cycles and the historically varying strength and size of rivers as barriers to dispersal may be the path to the answer to the long‐standing question of identifying the main drivers of Amazonian diversification.

     
    more » « less