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      Systematics, biogeography, and diversification of Scytalopus tapaculos (Rhinocryptidae), an enigmatic radiation of Neotropical montane birds

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          Abstract

          We studied the phylogeny, biogeography, and diversification of suboscine passerines in the genus Scytalopus (Rhinocryptidae), a widespread, species-rich, and taxonomically challenging group of Neotropical birds. We analyzed nuclear (exons, regions flanking ultraconserved elements) and mitochondrial (ND2) DNA sequence data for a taxonomically and geographically comprehensive sample of specimens collected from Costa Rica to Patagonia and Brazil. We found that Scytalopus is a monophyletic group sister to Eugralla and consists of 3 main clades roughly distributed in (1) the Southern Andes, (2) eastern Brazil, and (3) the Tropical Andes and Central America. The clades from the Southern Andes and eastern Brazil are sister to each other. Despite their confusing uniformity in plumage coloration, body shape, and overall appearance, rates of species accumulation through time in Scytalopus since the origin of the clade in the Late Miocene are unusually high compared with those of other birds, suggesting rapid non-adaptive diversification in the group. We attribute this to their limited dispersal abilities making them speciation-prone and their occurrence in a complex landscape with numerous barriers promoting allopatric differentiation. Divergence times among species and downturns in species accumulation rates in recent times suggest that most speciation events in Scytalopus predate climatic oscillations of the Pleistocene. Our analyses identified various cases of strong genetic structure within species and lack of monophyly of taxa, flagging populations which likely merit additional study to clarify their taxonomic status. In particular, detailed analyses of species limits are due in S. parvirostris, S. latrans, S. speluncae, the S. atratus complex, and the Southern Andes clade.

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          Ultraconserved elements anchor thousands of genetic markers spanning multiple evolutionary timescales.

          Although massively parallel sequencing has facilitated large-scale DNA sequencing, comparisons among distantly related species rely upon small portions of the genome that are easily aligned. Methods are needed to efficiently obtain comparable DNA fragments prior to massively parallel sequencing, particularly for biologists working with non-model organisms. We introduce a new class of molecular marker, anchored by ultraconserved genomic elements (UCEs), that universally enable target enrichment and sequencing of thousands of orthologous loci across species separated by hundreds of millions of years of evolution. Our analyses here focus on use of UCE markers in Amniota because UCEs and phylogenetic relationships are well-known in some amniotes. We perform an in silico experiment to demonstrate that sequence flanking 2030 UCEs contains information sufficient to enable unambiguous recovery of the established primate phylogeny. We extend this experiment by performing an in vitro enrichment of 2386 UCE-anchored loci from nine, non-model avian species. We then use alignments of 854 of these loci to unambiguously recover the established evolutionary relationships within and among three ancient bird lineages. Because many organismal lineages have UCEs, this type of genetic marker and the analytical framework we outline can be applied across the tree of life, potentially reshaping our understanding of phylogeny at many taxonomic levels.
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            Testing macro-evolutionary models using incomplete molecular phylogenies.

            Phylogenies reconstructed from gene sequences can be used to investigate the tempo and mode of species diversification. Here we develop and use new statistical methods to infer past patterns of speciation and extinction from molecular phylogenies. Specifically, we test the null hypothesis that per-lineage speciation and extinction rates have remained constant through time. Rejection of this hypothesis may provide evidence for evolutionary events such as adaptive radiations or key adaptations. In contrast to previous approaches, our methods are robust to incomplete taxon sampling and are conservative with respect to extinction. Using simulation we investigate, first, the adverse effects of failing to take incomplete sampling into account and, second, the power and reliability of our tests. When applied to published phylogenies our tests suggest that, in some cases, speciation rates have decreased through time.
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              Rates of speciation and morphological evolution are correlated across the largest vertebrate radiation.

              Several evolutionary theories predict that rates of morphological change should be positively associated with the rate at which new species arise. For example, the theory of punctuated equilibrium proposes that phenotypic change typically occurs in rapid bursts associated with speciation events. However, recent phylogenetic studies have found little evidence linking these processes in nature. Here we demonstrate that rates of species diversification are highly correlated with the rate of body size evolution across the 30,000+ living species of ray-finned fishes that comprise the majority of vertebrate biological diversity. This coupling is a general feature of fish evolution and transcends vast differences in ecology and body-plan organization. Our results may reflect a widespread speciational mode of character change in living fishes. Alternatively, these findings are consistent with the hypothesis that phenotypic 'evolvability'-the capacity of organisms to evolve-shapes the dynamics of speciation through time at the largest phylogenetic scales.
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                Author and article information

                Journal
                The Auk
                Oxford University Press (OUP)
                0004-8038
                1938-4254
                March 21 2020
                Affiliations
                [1 ]Departamento de Ciencias Biológicas, Universidad de los Andes, Bogotá, Colombia
                [2 ]Department of Ecology and Evolutionary Biology, Tulane University, New Orleans, Louisiana, USA
                [3 ]Museum of Natural Science and Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana, USA
                [4 ]Instituto de Ciencias Naturales, Universidad Nacional de Colombia, Bogotá, Colombia
                [5 ]Secão de Aves, Museu de Zoologia, Universidade de São Paulo, São Paulo, Brazil
                [6 ]Museum of Comparative Zoology and Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts, USA
                [7 ]Center for Macroecology, Evolution and Climate, Natural History Museum of Denmark, Copenhagen, Denmark
                [8 ]Cornell Lab of Ornithology, Ithaca, New York, USA
                [9 ]Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, Tennessee, USA
                Article
                10.1093/auk/ukz077
                © 2020

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