River network rearrangements promote speciation in lowland Amazonian birds

Musher, Lukas J.; Giakoumis, Melina; Albert, James S.; Del‐Rio, Glaucia; Rêgo, Marco Antonio; Aleixo, Alexandre Luis Padovan; Ribas, Camila C.; Brumfield, Robb T.; Smith, Brian Tilston; Cracraft, Joel

doi:10.1101/2021.11.15.468717

Cited by 10 publications

(11 citation statements)

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“…Although the role of rivers as primary or secondary barriers in the avian evolutionary process remains controversial (Naka and Brumfield, 2018), the fact that rivers do somehow limit dispersal and gene flow is well accepted (Haffer, 1992;Musher et al, 2022). In the last three decades, we have advanced considerably in gathering genetic evidence showing gene flow restrictions across rivers (Capparella, 1988(Capparella, , 1991Ribas et al, 2012), but we had made only minor advances in understanding the real limitations that current rivers impose on flying birds.…”

Section: Introductionmentioning

confidence: 99%

Riverine Barriers as Obstacles to Dispersal in Amazonian Birds

et al. 2022

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Amazonian rivers represent known barriers for avian dispersal, reducing gene flow and enhancing differentiation. Despite the importance of rivers in the avian evolutionary process, we have made only minor advances in understanding the limitations imposed by rivers on flying birds. To fill that gap, we conducted dispersal-challenge experiments over water, assessing the flying capabilities of 84 tropical bird species of 22 different avian families. We mist-netted and released 484 birds from a stationary boat on the Rio Branco, northern Amazonia, at increasing distances from the shore, including 249 individuals at 100; 219 at 200; 8 at 300; and 5 at 400 m. A successful trial was represented by a bird reaching the riverbank, whereas a failure would refer to birds not reaching the shore and landing on the water, when they were rescued by our team. Our main goal was to understand if the outcome in the experiments could be predicted by (i) phylogenetic constraints, (ii) morphology (body mass and wing shape), (iii) flight speed, (iv) ecological preferences (stratum, habitat, and river-island specialization), and (v) psychological reluctance to fly. Nearly two thirds of the individuals (332) were successful in reaching the riverbank, whereas 152 failed. We found significant differences among lineages. Whereas seven avian families succeeded in all of the trials, two families (antbirds and wrens) were particularly bad dispersers (<40% success). The hand-wing index (HWI) was the single most powerful predictor of trial success. Flying speed was also a significant predictor of success. Overall, ecological attributes had a low explanatory power. Only forest stratum preference had a significant, although weak, effect on dispersal ability: canopy- and ground-dwellers performed better than understory birds. However, we found no effect of habitat preference or river-island specialization on dispersal ability. Our speed estimates for 64 bird species are among the first produced for the tropics and suggest slower flying speeds than those reported from temperate migratory birds. Although birds showed behavioral differences when presented with the opportunity to fly away from the boat, we found no evidence that their reluctance to fly could predict the outcome in the experiments. This represents the first experimental study evaluating the riverine effect through dispersal ability of Amazonian birds, providing important insights to better understand dispersal limitations provided by riverine barriers.

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Section: Introductionmentioning

confidence: 99%

Riverine Barriers as Obstacles to Dispersal in Amazonian Birds

et al. 2022

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“…Although the probability for alternative topologies was more stable across the genomes of X. spixii and L. vociferans, topology weight was also predicted by recombination rate and gene flow. The conflicting phylogenetic pattern reported here might be common across the thousands of lineages isolated by Amazonian tributaries, given that recent studies have been suggesting extensive introgression across rivers (Barrera-Guzmán et al 2018;Berv et al 2021;Ferreira et al 2018;Del-Rio et al 2021;Weir et al 2015;Musher et al 2021).…”

Section: Genomic Architecture Informs Patterns Of Spatial Diversifica...mentioning

confidence: 65%

“…Support for topology 2 for P. nigromaculata would indicate that the taxa diverged via a stepping-stone process from the west through the Tapajos, Xingu, and Belem regions, consistent with the Moisture Gradient Hypothesis (Silva et al 2019). In contrast, if topology 1 reflects the population history of P. nigromaculata , it would indicate an opposite scenario, with an ancestral population in southeastern Amazonia, which could be linked to physiographic changes in the landscape (Musher et al 2021; Albert et al 2018). Although the probability for alternative topologies was more stable across the genomes of X. spixii and L. vociferans , topology weight was also predicted by recombination rate and gene flow.…”

Section: Discussionmentioning

confidence: 99%

“…The species isolated by large rivers show complex and highly variable relationships that span millions of years, with limited congruence in spatial patterns of diversification and historical demography (Smith et al 2014; Silva et al 2019). Reduced genomic approaches have revealed that factors such as gene flow may hinder inferences on the origins of species distributed across Amazonian rivers (Weir et al 2015; Barrera-Guzmán et al 2018; Berv et al 2021; Ferreira et al 2018; Luna et al 2021; Musher et al 2021; Del-Rio et al 2021). In addition to gene flow, intrinsic (e.g., recombination rate) and extrinsic (e.g., selection) processes that influence the landscape of genomic diversity and differentiation may further obfuscate biogeographic inferences by affecting the estimation of phylogenetic and demographic parameters (Bravo et al 2021; Harvey et al 2019).…”

Section: Introductionmentioning

confidence: 99%

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Genomic architecture drives population structuring in Amazonian birds

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et al. 2021

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Large rivers are ubiquitously invoked to explain the distributional limits and speciation of the Amazon Basin’s mega-diversity. However, inferences on the spatial and temporal origins of Amazonian species have narrowly focused on evolutionary neutral models, ignoring the potential role of natural selection and intrinsic genomic processes known to produce heterogeneity in differentiation across the genome. To test how these factors may influence evolutionary inferences across multiple taxa, we sequenced whole genomes of populations for three bird species that co-occur in southeastern Amazonian and exhibit different life histories linked to their propensity to maintain gene flow across the landscape. 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 the species tree topology weight. Gene flow was less pervasive in regions of low recombination, making these windows more suitable for commonly used phylogenetic methods that assume a bifurcating-branching model. To corroborate that these associations were attributable to selection, we modeled the signature of adaptive alleles across the genome taking demographic history into account, and found that on average 31.6 % of the genome showed high probability for patterns consistent with selective sweeps and linked selection directly affecting the estimation of evolutionary parameters. By implementing a comparative genomic approach we were able to disentangle the effects of intrinsic genomic characteristics and selection from the neutral processes and show how speciation hypotheses are sensitive to genomic architecture.

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“…The effect of these changes on biodiversity became known as the River Capture Hypothesis (Albert et al, 2018) and has shown great potential in the understanding of species distributions, particularly in fish. Recent studies have shown that river network rearrangements can also promote speciation in lowland Amazonian birds (Musher et al, 2022).…”

Section: Riverine Landscape Evolution and Diversificationmentioning

confidence: 99%

Editorial: The role of rivers in the origins, evolution, adaptation, and distribution of biodiversity

et al. 2022

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Editorial on the Research TopicThe role of rivers in the origins, evolution, adaptation, and distribution of biodiversity Rivers represent ubiquitous landscape features and affect biodiversity in fundamental ways. Not only do they provide the medium necessary to sustain aquatic life, but they also influence the structure and biodiversity of both riparian and non-riparian habitats. Therefore, rivers can potentially affect the origins, evolution, adaptation, and distribution of both aquatic and terrestrial biota. The goal of this Research Topic was to provide a forum to discuss recent advances in the study of the role of rivers in the ecology and evolution of biodiversity. Specifically, we aimed to highlight the current and historical role of rivers in the evolutionary process and reveal different ways by which rivers affect biodiversity. In this editorial, we will review (i) the role of rivers in the origin and evolution of species; (ii) how river reorganization can affect species diversity; (iii) the effect of riverine habitats as environmental filters; and (iv) the importance of community-based management for biodiversity conservation. Rivers and the origin and evolution of terrestrial speciesThe association of rivers with the speciation process in non-aquatic species can be traced back to Wallace's explorations in the Amazon, where he documented that several species of primates had closely related, yet morphologically different, populations across some major rivers (Wallace, 1852). These observations were subsequently interpreted as evidence of the vicariant force of rivers in the speciation process, a model that became known as the Riverine Barrier Hypothesis (Sick, 1967;Capparella, 1988Capparella, , 1991. Although there are many examples of rivers acting as biogeographical barriersFrontiers in Ecology and Evolution frontiersin.org

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River network rearrangements promote speciation in lowland Amazonian birds

Cited by 10 publications

References 95 publications

Riverine Barriers as Obstacles to Dispersal in Amazonian Birds

Riverine Barriers as Obstacles to Dispersal in Amazonian Birds

Genomic architecture drives population structuring in Amazonian birds

Editorial: The role of rivers in the origins, evolution, adaptation, and distribution of biodiversity

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