skip to main content


Title: A legacy of geo‐climatic complexity and genetic divergence along the lower Colorado River: Insights from the geological record and 33 desert‐adapted animals
Abstract Aim

To review the histories of the Colorado River and North American monsoon system to ascertain their effects on the genetic divergence of desert‐adapted animals.

Location

Lower Colorado River region, including Mojave and Sonoran deserts, United States.

Methods

We synthesized recent geological literature to summarize initiation phases of lower Colorado River evolution, their discrepancies, and potential for post‐vicariance dispersal of animals across the river. We simulated data under geological models and performed a meta‐analysis of published and unpublished genetic data including population diversity metrics, relatedness and historical migration rates to assess alternative divergence hypotheses.

Results

The two models for arrival of the Colorado River into the Gulf of California impose east‐west divergence ages of 5.3 and 4.8 Ma, respectively. We found quantifiable river‐associated differentiation in the lower Colorado River region in reptiles, arachnids and mammals relative to flying insects. However, topological statistics, historical migration rates and cross‐river extralimital populations suggest that the river should be considered a leaky barrier that filters, rather than prevents, gene flow. Most markers violated neutrality tests. Differential adaptation to monsoon‐based precipitation differences may contribute to divergence between Mojave and Sonoran populations and should be tested.

Main Conclusions

Rivers are dynamic features that can both limit and facilitate gene flow through time, the impacts of which are mitigated by species‐specific life history and dispersal traits. The Southwest is a geo‐climatically complex region with the potential to produce pseudocongruent patterns of genetic divergence, offering a good setting to evaluate intermediate levels of geological‐biological (geobiological) complexity.

 
more » « less
Award ID(s):
1754030
NSF-PAR ID:
10459483
Author(s) / Creator(s):
 ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Journal of Biogeography
Volume:
46
Issue:
11
ISSN:
0305-0270
Page Range / eLocation ID:
p. 2479-2505
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Aim: To review the histories of the Colorado River and North American monsoon system to ascertain their effects on the genetic divergence of desert‐adapted animals. Location: Lower Colorado River region, including Mojave and Sonoran deserts, United States. Methods: We synthesized recent geological literature to summarize initiation phases of lower Colorado River evolution, their discrepancies, and potential for post‐vicariance dispersal of animals across the river. We simulated data under geological models and performed a meta‐analysis of published and unpublished genetic data including population diversity metrics, relatedness and historical migration rates to assess alternative divergence hypotheses. Results: The two models for arrival of the Colorado River into the Gulf of California impose east‐west divergence ages of 5.3 and 4.8 Ma, respectively. We found quantifiable river‐associated differentiation in the lower Colorado River region in reptiles, arachnids and mammals relative to flying insects. However, topological statistics, historical migration rates and cross‐river extralimital populations suggest that the river should be considered a leaky barrier that filters, rather than prevents, gene flow. Most markers violated neutrality tests. Differential adaptation to monsoon‐based precipitation differences may contribute to divergence between Mojave and Sonoran populations and should be tested. Main Conclusions: Rivers are dynamic features that can both limit and facilitate gene flow through time, the impacts of which are mitigated by species‐specific life history and dispersal traits. The Southwest is a geo‐climatically complex region with the potential to produce pseudocongruent patterns of genetic divergence, offering a good setting to evaluate intermediate levels of geological‐biological (geobiological) complexity. 
    more » « less
  2. Abstract Aim

    To investigate the cryptic diversity and diversification timing in the putatively low‐dispersal Amazonian leaf‐litter lizardLoxopholis osvaldoi, and to ask how geography (rivers, isolation by distance, IBD), ecological drivers (isolation by environment, IBE) and historical factors (climatic refugia) explain intraspecific genetic variation.

    Location

    Central Amazonia, Brazil.

    Taxon

    Squamata; Gymnophthalmidae;Loxopholis osvaldoi.

    Methods

    We sequenced two mitochondrial and two nuclear markers in 157 individuals. Phylogeographic structure and the occurrence of independent evolving lineages where explored through phylogenetic and coalescent analyses. A species tree and divergence dates of lineages were inferred with *BEAST, employing multiple DNA substitution rates. The potential genetic impacts of geographical distance among localities, the environment and the position of localities in relation to main rivers were tested by redundancy analysis (RDA).

    Results

    We detected 11 independently evolving and largely divergent intraspecific lineages. Lineage distribution patterns are complex and do not match any conspicuous barrier to gene flow, except for the Amazon River. Most lineages appear to have originated in the lower Miocene and Pliocene, in disagreement with the Pleistocene refuge hypothesis. IBD, IBE and rivers appear to have acted in concert establishing and maintaining genetic structure. However, when controlling for other explanatory variables, IBD explains significantly more variation than rivers, IBE or historical factors.

    Main Conclusions

    Our results strongly suggest thatL.osvaldoiis a species complex. Future taxonomic work should use an integrative approach to explore whether morphological variation is present and congruent with the genetic data. While the use of a sensitive dating analysis allowed us to better describe the diversification history ofL.osvaldoi, the lack of a spatial model of Neogene river dynamics prevents the test of specific, more informative river barrier hypotheses. The data suggest that nonlinear correlation analyses (e.g. RDA) should be preferred to detect factors that affect phylogeographic patterns in the Amazon, instead of linear multiple regressions (e.g. Mantel tests). Given the high level of cryptic diversity detected within this and other Amazonian species, we caution against hypothesis tests based solely on the distribution of nominal taxa, which can provide a rather incomplete view of the processes behind Amazonian diversity.

     
    more » « less
  3. Abstract Aim

    Present Amazonian diversity patterns can result from many different mechanisms and, consequently, the factors contributing to divergence across regions and/or taxa may differ. Nevertheless, the river‐barrier hypothesis is still widely invoked as a causal process in divergence of Amazonian species. Here we use model‐based phylogeographic analyses to test the extent to which major Amazonian rivers act similarly as barriers across time and space in two broadly distributed Amazonian taxa.

    Local

    Amazon rain forest.

    Taxon

    The lizardGonatodes humeralis(Sphaerodactylidae) and the tree frogDendropsophus leucophyllatus(Hylidae).

    Methods

    We obtained RADseq data for samples distributed across main river barriers, representing main Areas of Endemism previously proposed for the region. We conduct model‐based phylogeographic and genetic differentiation analyses across each population pair.

    Results

    Measures of genetic differentiation (based onFSTcalculated from genomic data) show that all rivers are associated with significant genetic differentiation. Parameters estimated under investigated divergence models showed that divergence times for populations separated by each of the 11 bordering rivers were all fairly recent. The degree of differentiation consistently varied between taxa and among rivers, which is not an artifact of any corresponding difference in the genetic diversities of the respective taxa, or to amounts of migration based on analyses of the site‐frequency spectrum.

    Main conclusions

    Taken together, our results support a dispersal (rather than vicariance) history, without strong evidence of congruence between these species and rivers. However, once a species crossed a river, populations separated by each and every river have remained isolated—in this sense, rivers act similarly as barriers to any further gene flow. This result suggests differing degrees of persistence and gives rise to the seeming contradiction that the divergence process indeed varies across time, space and species, even though major Amazonian rivers have acted as secondary barriers to gene flow in the focal taxa.

     
    more » « less
  4. Abstract Aim

    To investigate the structure and rate of gene flow among populations of habitat‐specialized species to understand the ecological and evolutionary processes underpinning their population dynamics and historical demography, including speciation and extinction.

    Location

    Peruvian and Argentine Andes.

    Taxon

    Two subspecies of torrent duck (Merganetta armata).

    Methods

    We sampled 156 individuals in Peru (M. a. leucogenis;Chillón River,n = 57 and Pachachaca River,n = 49) and Argentina (M. a. armata;Arroyo Grande River,n = 33 and Malargüe River,n = 17), and sequenced the mitochondrial DNA (mtDNA) control region to conduct coarse and fine‐scale demographic analyses of population structure. Additionally, to test for differences between subspecies, and across genetic markers with distinct inheritance patterns, a subset of individuals (Peru,n = 10 and Argentina,n = 9) was subjected to partial genome resequencing, obtaining 4,027 autosomal and 189 Z‐linked double‐digest restriction‐associated DNA sequences.

    Results

    Haplotype and nucleotide diversities were higher in Peru than Argentina across all markers. Peruvian and Argentine subspecies showed concordant species‐level differences (ΦSTmtDNA = 0.82; ΦSTautosomal = 0.30; ΦSTZ chromosome = 0.45), including no shared mtDNA haplotypes. Demographic parameters estimated for mtDNA using IM and IMa2 analyses, and for autosomal markers using∂a∂i(isolation‐with‐migration model), supported an old divergence (mtDNA = 600,000 years before present (ybp), 95% HPD range = 1.2 Mya to 200,000 ybp; and autosomal∂a∂i = 782,490 ybp), between the two subspecies, characteristic of deeply diverged lineages. The populations were well‐differentiated in Argentina but moderately differentiated in Peru, with low unidirectional gene flow in each country.

    Main conclusions

    We suggest that the South American Arid Diagonal was preexisting and remains a current phylogeographic barrier between the ranges of the two torrent duck subspecies, and the adult territoriality and breeding site fidelity to the rivers define their population structure.

     
    more » « less
  5. Abstract

    The opposing forces of gene flow and isolation are two major processes shaping genetic diversity. Understanding how these vary across space and time is necessary to identify the environmental features that promote diversification. The detection of considerable geographic structure in taxa from the arid Nearctic has prompted research into the drivers of isolation in the region. Several geographic features have been proposed as barriers to gene flow, including the Colorado River, Western Continental Divide (WCD), and a hypothetical Mid-Peninsular Seaway in Baja California. However, recent studies suggest that the role of barriers in genetic differentiation may have been overestimated when compared to other mechanisms of divergence. In this study, we infer historical and spatial patterns of connectivity and isolation in Desert Spiny Lizards (Sceloporus magister) and Baja Spiny Lizards (Sceloporus zosteromus), which together form a species complex composed of parapatric lineages with wide distributions in arid western North America. Our analyses incorporate mitochondrial sequences, genomic-scale data, and past and present climatic data to evaluate the nature and strength of barriers to gene flow in the region. Our approach relies on estimates of migration under the multispecies coalescent to understand the history of lineage divergence in the face of gene flow. Results show that the S. magister complex is geographically structured, but we also detect instances of gene flow. The WCD is a strong barrier to gene flow, while the Colorado River is more permeable. Analyses yield conflicting results for the catalyst of differentiation of peninsular lineages in S. zosteromus. Our study shows how large-scale genomic data for thoroughly sampled species can shed new light on biogeography. Furthermore, our approach highlights the need for the combined analysis of multiple sources of evidence to adequately characterize the drivers of divergence.

     
    more » « less