Title: Giant Tree Frog diversification in West and Central Africa: Isolation by physical barriers, climate, and reproductive traits
Abstract
Secondary sympatry amongst sister lineages is strongly associated with genetic and ecological divergence. This pattern suggests that for closely related species to coexist in secondary sympatry, they must accumulate differences in traits that mediate ecological and/or reproductive isolation. Here, we characterized inter‐ and intraspecific divergence in three giant tree frog species whose distributions stretch across West and Central Africa. Using genome‐wide single‐nucleotide polymorphism data, we demonstrated that species‐level divergence coincides temporally and geographically with a period of large‐scale forest fragmentation during the late Pliocene. Our environmental niche models further supported a dynamic history of climatic suitability and stability, and indicated that all three species occupy distinct environmental niches. We found modest morphological differentiation amongst the species with significant divergence in tympanum diameter and male advertisement call. In addition, we confirmed that two species occur in secondary sympatry in Central Africa but found no evidence of hybridization. These patterns support the hypothesis that cycles of genetic exchange and isolation across West and Central Africa have contributed to globally significant biodiversity. Furthermore, divergence in both ecology and reproductive traits appear to have played important roles in maintaining distinct lineages. At the intraspecific level, we found that climatic refugia, precipitation gradients, marine incursions, and potentially riverine barriers generated phylogeographic structure throughout the Pleistocene and into the Holocene. Further studies examining phenotypic divergence and secondary contact amongst these geographically structured populations may demonstrate how smaller scale and more recent biogeographic barriers contribute to regional diversification.
Leaché, Adam D.; Portik, Daniel M.; Rivera, Danielle; Rödel, Mark‐Oliver; Penner, Johannes; Gvoždík, Václav; Greenbaum, Eli; Jongsma, Gregory F. M.; Ofori‐Boateng, Caleb; Burger, Marius; et al(
, Journal of Biogeography)
AbstractAim
Species with wide distributions spanning the African Guinean and Congolian rain forests are often composed of genetically distinct populations or cryptic species with geographic distributions that mirror the locations of the remaining forest habitats. We used phylogeographic inference and demographic model testing to evaluate diversification models in a widespread rain forest species, the African foam‐nest treefrogChiromantis rufescens.
Location
Guinean and Congolian rain forests, West and Central Africa.
Taxon
Chiromantis rufescens.
Methods
We collected mitochondrial DNA (mtDNA) and single‐nucleotide polymorphism (SNP) data for 130 samples ofC. rufescens. After estimating population structure and inferring species trees using coalescent methods, we tested demographic models to evaluate alternative population divergence histories that varied with respect to gene flow, population size change and periods of isolation and secondary contact. Species distribution models were used to identify the regions of climatic stability that could have served as forest refugia since the last interglacial.
Results
Population structure withinC. rufescensresembles the major biogeographic regions of the Guinean and Congolian forests. Coalescent‐based phylogenetic analyses provide strong support for an early divergence between the western Upper Guinean forest and the remaining populations. Demographic inferences support diversification models with gene flow and population size changes even in cases where contemporary populations are currently allopatric, which provides support for forest refugia and barrier models. Species distribution models suggest that forest refugia were available for each of the populations throughout the Pleistocene.
Main conclusions
Considering historical demography is essential for understanding population diversification, especially in complex landscapes such as those found in the Guineo–Congolian forest. Population demographic inferences help connect the patterns of genetic variation to diversification model predictions. The diversification history ofC. rufescenswas shaped by a variety of processes, including vicariance from river barriers, forest fragmentation and adaptive evolution along environmental gradients.
Anderson, Carlie B.; Ospina, Oscar; Beerli, Peter; Lemmon, Alan R.; Banker, Sarah E.; Hassinger, Alyssa Bigelow; Dye, Mysia; Kortyna, Michelle L.; Lemmon, Emily Moriarty(
, Ecology and Evolution)
Abstract
Species interactions drive diverse evolutionary outcomes. Speciation by cascade reinforcement represents one example of how species interactions can contribute to the proliferation of species. This process occurs when the divergence of mating traits in response to selection against interspecific hybridization incidentally leads to reproductive isolation among populations of the same species. Here, we investigated the population genetic outcomes of cascade reinforcement in North American chorus frogs (Hylidae:Pseudacris). Specifically, we estimated the frequency of hybridization among three taxa, assessed genetic structure within the focal species,P.feriarum, and ascertained the directionality of gene flow withinP.feriarumacross replicated contact zones via coalescent modeling. Through field observations and preliminary experimental crosses, we assessed whether hybridization is possible under natural and laboratory conditions. We found that hybridization occurs amongP.feriarumand two conspecifics at a low rate in multiple contact zones, and that gene flow within the former species is unidirectional from allopatry into sympatry with these other species in three of four contact zones studied. We found evidence of substantial genetic structuring withinP.feriarumincluding a divergent western allopatric cluster, a behaviorally‐distinct sympatric South Carolina cluster, and several genetically‐overlapping clusters from the remainder of the distribution. Furthermore, we found sub‐structuring between reinforced and nonreinforced populations in the two most intensely‐sampled contact zones. Our literature review indicated thatP.feriarumhybridizes with at least five heterospecifics at the periphery of its range providing a mechanism for further intraspecific diversification. This work strengthens the evidence for cascade reinforcement in this clade, revealing the geographic and genetic landscape upon which this process can contribute to the proliferation of species.
Brunton, Aaron J.; Farleigh, Keaka; Ogbourne, Steven M.; Rossetto, Maurizio; Schoeman, David S.; Conroy, Gabriel C.(
, Landscape Ecology)
AbstractContext
Processes that shape genomic and ecological divergence can reveal important evolutionary dynamics to inform the conservation of threatened species.Fontaineais a genus of rainforest shrubs and small trees including critically endangered and threatened species restricted to narrow, but complex geographic and ecological regions. Several species ofFontaineaare subject to spatially explicit conditions and experience limited intra-specific gene flow, likely generating genetic differentiation and local adaptation.
Objectives
Here, we explored the genetic and ecological mechanisms underlying patterns of diversification in two, closely related threatenedFontaineaspecies. Our aim was to compare spatial patterns of genetic variation between the vulnerableFontainea australis(Southern Fontainea) and critically endangeredF. oraria(Coastal Fontainea), endemic to the heterogeneous subtropical region of central, eastern Australia, where large-scale clearing has severely reduced rainforest habitat to a fraction (< 1%) of its pre-European settlement extent.
Methods
We used a set of 10,000 reduced-representation markers to infer genetic relationships and the drivers of spatial genetic variation across the two species. In addition, we employed a combination of univariate and multivariate genome-environment association analysis using a set of topo-climatic variables to explore potential patterns of local adaptation as a factor impacting genomic divergence.
Results
Our study revealed that Coastal Fontainea have a close genetic relationship with Southern Fontainea. We showed that isolation by distance has played a key role in their genetic variation, indicating that vicariance can explain the spatial genetic distribution of the two species. Genotype-environment analyses showed a strong association with temperature and topographic features, suggesting adaptation to localised thermal environments. We used a multivariate redundancy analysis to identify a range of putatively adapted loci associated with local environmental conditions.
Conclusions
Divergent selection at the local-habitat scale as a result of dispersal limitations and environmental heterogeneity (including physical barriers) are likely contributors to adaptive divergence between the twoFontaineaspecies. Our findings have presented evidence to indicate that Southern and Coastal Fontainea were comprised of distinct genetic groups and ecotypes, that together may form a single species continuum, with further phenotype research suggested to confirm the current species boundaries. Proactive conservation actions, including assisted migration to enhance the resilience of populations lacking stress-tolerant single nucleotide polymorphisms (SNPs) may be required to secure the long-term future of both taxa. This is especially vital for the critically endangered Coastal Fontainea given projections of habitat decline for the species under future climate scenarios.
Pavón-Vázquez, Carlos J.; Rana, Qaantah; Farleigh, Keaka; Crispo, Erika; Zeng, Mimi; Liliah, Jeevanie; Mulcahy, Daniel; Ascanio, Alfredo; Jezkova, Tereza; Leaché, Adam D.; et al(
, Systematic Biology)
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.
Titus, Benjamin M.; Daly, Marymegan; Hamilton, Natalie; Berumen, Michael L.; Baeza, J. Antonio(
, Journal of Biogeography)
AbstractAim
The “sexy shrimp”Thor amboinensisis currently considered a single circumtropical species. However, the tropical oceans are partitioned by hard and soft barriers to dispersal, providing ample opportunity for allopatric speciation. Herein, we test the null hypothesis thatT. amboinensisis a single global species, reconstruct its global biogeographical history, and comment on population‐level patterns throughout the Tropical Western Atlantic.
Location
Coral reefs in all tropical oceans.
Methods
Specimens ofThor amboinensiswere obtained through field collection and museum holdings. We used one mitochondrial (COI) and two nuclear (NaK, enolase) gene fragments for global species delimitation and phylogenetic analyses (n = 83 individuals, 30 sample localities), while phylogeographical reconstruction in theTWAwas based onCOIonly (n = 303 individuals, 10 sample localities).
Results
We found evidence for at least five cryptic lineages (9%–22%COIpairwise sequence divergence): four in the Indo‐West Pacific and one in the Tropical Western Atlantic. Phylogenetic reconstruction revealed that endemic lineages from Japan and the South Central Pacific are more closely related to the Tropical Western Atlantic lineage than to a co‐occurring lineage that is widespread throughout the Indo‐West Pacific. Concatenated and species tree phylogenetic analyses differ in the placement of an endemic Red Sea lineage and suggest alternate dispersal pathways into the Atlantic. Phylogeographical reconstruction throughout the Tropical Western Atlantic reveals little genetic structure over more than 3,000 km.
Main conclusions
Thor amboinensisis a species complex that has undergone a series of allopatric speciation events and whose members are in secondary contact in the Indo‐West Pacific. Nuclear‐ and mitochondrial‐ gene phylogenies show evidence of introgression between lineages inferred to have been separated more than 20 Ma. Phylogenetic discordance between multi‐locus analyses suggest thatT. amboinensisoriginated in the Tethys sea and dispersed into the Atlantic and Indo‐West Pacific through the Tethys seaway or, alternatively, originated in the Indo‐West Pacific and dispersed into the Atlantic around South Africa. Population‐level patterns in the Caribbean indicate extensive gene flow across the region.
Jaynes, Kyle E., Myers, Edward A., Gvoždík, Václav, Blackburn, David C., Portik, Daniel M., Greenbaum, Eli, Jongsma, Gregory F. M., Rödel, Mark‐Oliver, Badjedjea, Gabriel, Bamba‐Kaya, Abraham, Baptista, Ninda L., Akuboy, Jeannot B., Ernst, Raffael, Kouete, Marcel T., Kusamba, Chifundera, Masudi, Franck M., McLaughlin, Patrick J., Nneji, Lotanna M., Onadeko, Abiodun B., Penner, Johannes, Vaz Pinto, Pedro, Stuart, Bryan L., Tobi, Elie, Zassi‐Boulou, Ange‐Ghislain, Leaché, Adam D., Fujita, Matthew K., and Bell, Rayna C. Giant Tree Frog diversification in West and Central Africa: Isolation by physical barriers, climate, and reproductive traits. Molecular Ecology 31.15 Web. doi:10.1111/mec.16169.
Jaynes, Kyle E., Myers, Edward A., Gvoždík, Václav, Blackburn, David C., Portik, Daniel M., Greenbaum, Eli, Jongsma, Gregory F. M., Rödel, Mark‐Oliver, Badjedjea, Gabriel, Bamba‐Kaya, Abraham, Baptista, Ninda L., Akuboy, Jeannot B., Ernst, Raffael, Kouete, Marcel T., Kusamba, Chifundera, Masudi, Franck M., McLaughlin, Patrick J., Nneji, Lotanna M., Onadeko, Abiodun B., Penner, Johannes, Vaz Pinto, Pedro, Stuart, Bryan L., Tobi, Elie, Zassi‐Boulou, Ange‐Ghislain, Leaché, Adam D., Fujita, Matthew K., & Bell, Rayna C. Giant Tree Frog diversification in West and Central Africa: Isolation by physical barriers, climate, and reproductive traits. Molecular Ecology, 31 (15). https://doi.org/10.1111/mec.16169
Jaynes, Kyle E., Myers, Edward A., Gvoždík, Václav, Blackburn, David C., Portik, Daniel M., Greenbaum, Eli, Jongsma, Gregory F. M., Rödel, Mark‐Oliver, Badjedjea, Gabriel, Bamba‐Kaya, Abraham, Baptista, Ninda L., Akuboy, Jeannot B., Ernst, Raffael, Kouete, Marcel T., Kusamba, Chifundera, Masudi, Franck M., McLaughlin, Patrick J., Nneji, Lotanna M., Onadeko, Abiodun B., Penner, Johannes, Vaz Pinto, Pedro, Stuart, Bryan L., Tobi, Elie, Zassi‐Boulou, Ange‐Ghislain, Leaché, Adam D., Fujita, Matthew K., and Bell, Rayna C.
"Giant Tree Frog diversification in West and Central Africa: Isolation by physical barriers, climate, and reproductive traits". Molecular Ecology 31 (15). Country unknown/Code not available: Wiley-Blackwell. https://doi.org/10.1111/mec.16169.https://par.nsf.gov/biblio/10375203.
@article{osti_10375203,
place = {Country unknown/Code not available},
title = {Giant Tree Frog diversification in West and Central Africa: Isolation by physical barriers, climate, and reproductive traits},
url = {https://par.nsf.gov/biblio/10375203},
DOI = {10.1111/mec.16169},
abstractNote = {Abstract Secondary sympatry amongst sister lineages is strongly associated with genetic and ecological divergence. This pattern suggests that for closely related species to coexist in secondary sympatry, they must accumulate differences in traits that mediate ecological and/or reproductive isolation. Here, we characterized inter‐ and intraspecific divergence in three giant tree frog species whose distributions stretch across West and Central Africa. Using genome‐wide single‐nucleotide polymorphism data, we demonstrated that species‐level divergence coincides temporally and geographically with a period of large‐scale forest fragmentation during the late Pliocene. Our environmental niche models further supported a dynamic history of climatic suitability and stability, and indicated that all three species occupy distinct environmental niches. We found modest morphological differentiation amongst the species with significant divergence in tympanum diameter and male advertisement call. In addition, we confirmed that two species occur in secondary sympatry in Central Africa but found no evidence of hybridization. These patterns support the hypothesis that cycles of genetic exchange and isolation across West and Central Africa have contributed to globally significant biodiversity. Furthermore, divergence in both ecology and reproductive traits appear to have played important roles in maintaining distinct lineages. At the intraspecific level, we found that climatic refugia, precipitation gradients, marine incursions, and potentially riverine barriers generated phylogeographic structure throughout the Pleistocene and into the Holocene. Further studies examining phenotypic divergence and secondary contact amongst these geographically structured populations may demonstrate how smaller scale and more recent biogeographic barriers contribute to regional diversification.},
journal = {Molecular Ecology},
volume = {31},
number = {15},
publisher = {Wiley-Blackwell},
author = {Jaynes, Kyle E. and Myers, Edward A. and Gvoždík, Václav and Blackburn, David C. and Portik, Daniel M. and Greenbaum, Eli and Jongsma, Gregory F. M. and Rödel, Mark‐Oliver and Badjedjea, Gabriel and Bamba‐Kaya, Abraham and Baptista, Ninda L. and Akuboy, Jeannot B. and Ernst, Raffael and Kouete, Marcel T. and Kusamba, Chifundera and Masudi, Franck M. and McLaughlin, Patrick J. and Nneji, Lotanna M. and Onadeko, Abiodun B. and Penner, Johannes and Vaz Pinto, Pedro and Stuart, Bryan L. and Tobi, Elie and Zassi‐Boulou, Ange‐Ghislain and Leaché, Adam D. and Fujita, Matthew K. and Bell, Rayna C.},
}
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