Biogeography of squirrel monkeys (genus Saimiri): South-central Amazon origin and rapid pan-Amazonian diversification of a lowland primate

Alfaro, Jessica W. Lynch; Boubli, Jean P.; Paim, Fernanda Pozzan; Ribas, Camila C.; Silva, Maria Nazareth F. da; Messias, Mariluce Rezende; Röhe, Fábio; Mercês, Michelle Pinto; Júnior, José S. Silva; Silva, Claudia R; Pinho, Gabriela Medeiros de; Koshkarian, Gohar; Nguyen, Mai Thi; Harada, Maria Lúcia; Rabelo, Rafael M.; Queiroz, Helder Lima de; Alfaro, Michael E.; Farias, Izeni Pires

doi:10.1016/j.ympev.2014.09.004

Cited by 144 publications

(101 citation statements)

References 51 publications

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“…Our work shows that the rivers indeed act as barriers restricting gene flow (Cowman & Bellwood, ; Naka & Brumfield, ). However, with the divergence times of each river varying, and the relative divergence times differing between species, our work supports the contention that the barriers represented by rivers may be much more dynamic than classic views of vicariant histories promoted by river formation (Lynch et al, ; Ribas et al, ). Moreover, by detailing how genetic divergence varies temporally, spatially and across taxa, our work lends support to the hypothesized proposal of cyclical periods of connections and isolations (i.e.…”

Section: Resultssupporting

confidence: 83%

“…The role of rivers in preventing gene flow and promoting diversification is supported by the existence of AoEs, such as those delimited by the borders of major Amazonian rivers, and which are supported by diversity patterns of different taxonomic groups (Fernandes et al, ; Godinho & da Silva, ; Lynch Alfaro et al, ). Our work extends these findings to population divergence of frogs and lizards, but we cannot predict if the observed genetic structure of D. leucophyllatus and G. humeralis associated with river barriers could promote speciation in these taxa over time (Sukumaran & Knowles, ).…”

Section: Discussionmentioning

confidence: 99%

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Testing main Amazonian rivers as barriers across time and space within widespread taxa

Pirani

Werneck

Thomaz

et al. 2019

Journal of Biogeography

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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 lizard Gonatodes humeralis (Sphaerodactylidae) and the tree frog Dendropsophus 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 on FST calculated 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.

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Section: Resultssupporting

confidence: 83%

Section: Discussionmentioning

confidence: 99%

Testing main Amazonian rivers as barriers across time and space within widespread taxa

Pirani

Werneck

Thomaz

et al. 2019

Journal of Biogeography

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“…In fact, these authors concluded that this genus comprises only three species, S. oerstedi , S. sciureus , and Saimiri vanzolinii , which diversified during the Pleistocene. This is consistent with the estimate of Alfaro et al (2015), who concluded that S. boliviensis diverged from the other Saimiri species less than 1.5 Ma.…”

supporting

confidence: 92%

“…This genus is distributed primarily in the Amazon basin and Guianas (Figure 1), except Saimiri oerstedii , which is found in Central America, Costa Rica and Panama (Chiou et al , 2011). One of the most recent biogeographical studies of Saimiri (Alfaro et al , 2015) indicated that the species diversity of the genus is the product of a recent pan-Amazonian radiation. Based on the 14 clades identified in the analysis of the mitochondrial DNA (D-loop and cytb), these authors suggested a provisional taxonomy consisting of S. sciureus , S. oerstedii ( S. o. oerstedii and S. o. citronellus ), S. collinsi , S. ustus (A, B, and C lineages), S. boliviensis, S. cassiquiarensis ( S. c. cassiquiarensis, S. c. albigena, S. c. macrodon A, S. c. macrodon B, and S. c. macrodon C), and S. vanzolinii .…”

mentioning

confidence: 99%

Molecular data highlight hybridization in squirrel monkeys (Saimiri, Cebidae)

et al. 2016

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Hybridization has been reported increasingly frequently in recent years, fueling the debate on its role in the evolutionary history of species. Some studies have shown that hybridization is very common in captive New World primates, and hybrid offspring have phenotypes and physiological responses distinct from those of the "pure" parents, due to gene introgression. Here we used the TA15 Alu insertion to investigate hybridization in the genus Saimiri. Our results indicate the hybridization of Saimiri boliviensis peruviensis with S. sciureus macrodon, and S. b. boliviensis with S. ustus. Unexpectedly, some hybrids of both S. boliviensis peruviensis and S. b. boliviensis were homozygous for the absence of the insertion, which indicates that the hybrids were fertile.

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“…This formation could have similarly influenced capybaras. The HRCH seems to play a fundamental role in the diversification process of numerous avian taxa [11,[204][205][206][207][208][209] and some Primates taxa [110,210]. The temporal splits obtained with the MNJ procedure could also support the RH, because glacially-driven diversification mainly occurred within the last 0.9-0.02 MYA.…”

Section: Miocene and Pliocene Amazon Biodiversity Hypotheses For The mentioning

confidence: 95%

Continuous Miocene, Pliocene and Pleistocene Influences on Mitochondrial Diversification of the Capybara (Hydrochoerus Hydrochoeris; Hydrochoeridae, Rodentia): Incapacity to Determine Exclusive Hypotheses on the Origins of the Amazon and Orinoco Diversity for This Species

Ruiz‐García¹,

Luengas-Villamil²,

Pinedo-Castro³

et al. 2016

J Phylogenetics Evol Biol

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The capybara (Hydrochoerus hydrochoeris) is the largest rodent on the world and it is strongly linked to the river systems of a large fraction of South America and part of Central America (Panama). Thus, it is an interesting species to test hypotheses about the origin of the high biodiversity within the Amazon Basin and in a sizeable fraction of the Neotropics. To test these hypotheses, we sequenced two mitochondrial genes (control region and Cytochrome b) of 78 wild capybaras sampled in Colombia, Peru, Ecuador and Brazil. At least, five different "populations" or ESUs were detected in well delimited geographical areas. However, our results do not support the more recent view that two different species of capybara are present (H. hydrochoeris and H. isthmus), unless chromosomal speciation (stasipatric or parapatric) can be demonstrated between these two groups. A Bayesian tree with the aforementioned two mitochondrial genes, and another Bayesian tree with a subset of 25 capybaras for 10 mitochondrial genes, showed that the initial diversification of the mitochondrial haplotype in capybaras was initiated in the Late Miocene. The trees also showed that the other haplotype diversification processes extended into the Pliocene and Pleistocene. We also detected population expansion events during different moments of the Pleistocene. Although some authors strongly suggest that the Miocene diversification explains the extreme biodiversity in the Amazon Basin and in surroundings areas (for instance, the Paleogeography hypothesis), others consider it the result of available forest refugia (Refuge hypothesis) during the Pleistocene. However, our results suggest that both hypotheses (and others, such as the Riverrefuge, the Recent Lagoon and the Hydrogeological Recent Change hypotheses) could have affected the evolution of the capybara to generate the current mitochondrial diversity. Thus, it is difficult to generalize a unique Amazon biota diversification hypothesis because each species or taxon could be affected by different processes and because the temporal antiquity of each taxon in South America is also different. Many mammalian taxa, and others, migrated into South America during the Great American Biotic Interchange (GABI) and their diversification processes in South America were mainly driven by Pleistocene events as those proposed by the Refuge hypothesis. Older taxa within this continent could have begun their current genetics diversification processes earlier, such as in the case of the capybara.

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Biogeography of squirrel monkeys (genus Saimiri): South-central Amazon origin and rapid pan-Amazonian diversification of a lowland primate

Cited by 144 publications

References 51 publications

Testing main Amazonian rivers as barriers across time and space within widespread taxa

Testing main Amazonian rivers as barriers across time and space within widespread taxa

Molecular data highlight hybridization in squirrel monkeys (Saimiri, Cebidae)

Continuous Miocene, Pliocene and Pleistocene Influences on Mitochondrial Diversification of the Capybara (Hydrochoerus Hydrochoeris; Hydrochoeridae, Rodentia): Incapacity to Determine Exclusive Hypotheses on the Origins of the Amazon and Orinoco Diversity for This Species

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