skip to main content

Title: Unmasking hidden genetic, vocal, and size variation in the Masked Flowerpiercer along the Andes supports two species separated by Northern Peruvian Low

Genetic divergence among isolated populations is not always reflected in phenotypic differentiation. We investigated the genetic and phenotypic differentiation in Diglossa cyanea (Thraupidae; Masked Flowerpiercer), a widely distributed species in the tropical Andes. We found strong evidence for 2 main lineages separated by the Marañón River valley in the Northern Peruvian Low (NPL). These 2 lineages show a deep sequence divergence in mitochondrial DNA (mtDNA; ~6.7% uncorrected p-distance, n = 122), spectral frequency and song structure (with exclusive final whistles in southern populations, n = 88), and wing length (the northern populations are smaller, n = 364). The 2 divergent D. cyanea mitochondrial lineages were not sister to each other, suggesting a possible paraphyly with respect to D. caerulescens (Bluish Flowerpiercer) that remains to be tested with nuclear genomic data. No genetic variation, size difference, or song structure was observed within the extensive range of the southern group (from the NPL to central Bolivia) or within all sampled northern populations (from the NPL to Venezuela). These vocal differences appear to have consequences for song discrimination, and species recognition, according to a previously published playback experiment study. We propose that the southern taxon be elevated to species rank as D. melanopis, a monotypic species (with the proposed name Whistling Masked-Flowerpiercer). In turn, we provide a redefinition of D. cyanea (Warbling Masked-Flowerpiercer), which is now restricted to the northern half of the tropical Andes as a polytypic species with 3 subspecies (tovarensis, obscura, and cyanea). Based on our results, the subspecies dispar should be treated as a junior synonym of cyanea. Our study highlights the need to continue amassing complementary data sets from field observations, experiments, and collection-based assessments to better characterize the evolutionary history, biogeography, bioacoustics, and taxonomy of Neotropical montane birds.

more » « less
Author(s) / Creator(s):
; ; ; ;
Publisher / Repository:
Oxford University Press
Date Published:
Journal Name:
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Few studies have quantified the extent of genetic differentiation within widely distributed polytypic African bird species with disjunct ranges. Current knowledge indicates that high levels of genetic differentiation are found for such lineages but generalization of the pattern requires further comparisons with other co‐distributed taxa. We assessed the extent of phylogeographical structure across the range of the Olive WoodpeckerDendropicos griseocephalususing mitochondrial and nuclear intron data. The Olive Woodpecker occupies the forests of Central (Dendropicos griseocephalus ruwenzori) and Eastern (Dendropicos g. kilimensis) Africa, with a disjunct morphological lineage (Dendropicos g. griseocephalus) occurring in southern Africa. Each of the subspecies lineages can be diagnosed using morphology. Phylogenetic analyses of our sequence data recovered three monophyletic lineages withkilimensissister toruwenzori, andgriseocephalusas sister to the clade uniting these two taxa. Molecular species delimitation methods and estimates of gene flow under the isolation‐with‐migration model suggest that the clade uniting the central and eastern subspecies may be recognized as distinct at the species level from the nominate subspecies, which is restricted to southern Africa. We conclude thatD. griseocephalus(Boddaert, 1783) andD. ruwenzori(Sharpe, 1902) (including subspecieskilimensis) should be considered full species. The biogeographical pattern we uncover for the Olive Woodpecker differs from that of other co‐distributed widespread species both in terms of the order of sequence divergence of lineages occupying different areas of endemism in Africa, and in the timing of divergence, being younger (0.5–0.7 mya BP) than that recovered for the co‐distributed Square‐tailed DrongoDicrurus ludwigii(0.9–1.6 mya BP).

    more » « less
  2. Abstract

    Birds living in riverine environments may show weak population structure because high dispersal abilities required to track habitat dynamics can result in gene flow over broad spatial scales. Alternatively, the configuration of river networks may result in restricted dispersal within river courses or basins, leading to high genetic structure. Although several bird species are riverine specialists in the Andes, no study has extensively evaluated the population genetic structure of any of them. We examined evidence from genetic and morphological data to address questions about the biogeography and taxonomy of the Torrent Duck (Merganetta armata), a riverine specialist bird with a broad distribution in Andean riverine habitats which certainly comprises different subspecies and may comprise more than one species. We found deep subdivisions of Torrent Duck populations from the northern, central and southern portions of the Andes. These lineages, which partly coincide with subspecies described based on plumage variation and body size, do not share mtDNA haplotypes, have private nuclear alleles and exhibit marked differences in morphometric traits. Some geographic barriers presumably restricting gene flow between groups partially coincide with those associated with major genetic breaks in forest species with similar distributions along the Andes, suggesting that bird assemblages including species occupying different habitats were likely affected by common biogeographical events. The three groups of Torrent Ducks may be considered different species under some species definitions and are distinct evolutionary lineages to be conserved and managed separately.

    more » « less
  3. 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.


    Peruvian and Argentine Andes.


    Two subspecies of torrent duck (Merganetta armata).


    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.


    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
  4. Abstract

    Numerous mechanisms can drive speciation, including isolation by adaptation, distance, and environment. These forces can promote genetic and phenotypic differentiation of local populations, the formation of phylogeographic lineages, and ultimately, completed speciation. However, conceptually similar mechanisms may also result in stabilizing rather than diversifying selection, leading to lineage integration and the long‐term persistence of population structure within genetically cohesive species. Processes that drive the formation and maintenance of geographic genetic diversity while facilitating high rates of migration and limiting phenotypic differentiation may thereby result in population genetic structure that is not accompanied by reproductive isolation. We suggest that this framework can be applied more broadly to address the classic dilemma of “structure” versus “species” when evaluating phylogeographic diversity, unifying population genetics, species delimitation, and the underlying study of speciation. We demonstrate one such instance in the Seepage Salamander (Desmognathus aeneus) from the southeastern United States. Recent studies estimated up to 6.3% mitochondrial divergence and four phylogenomic lineages with broad admixture across geographic hybrid zones, which could potentially represent distinct species supported by our species‐delimitation analyses. However, while limited dispersal promotes substantial isolation by distance, microhabitat specificity appears to yield stabilizing selection on a single, uniform, ecologically mediated phenotype. As a result, climatic cycles promote recurrent contact between lineages and repeated instances of high migration through time. Subsequent hybridization is apparently not counteracted by adaptive differentiation limiting introgression, leaving a single unified species with deeply divergent phylogeographic lineages that nonetheless do not appear to represent incipient species.

    more » « less
  5. Phylogenomic investigations of biodiversity facilitate the detection of fine-scale population genetic structure and the demographic histories of species and populations. However, determining whether or not the genetic divergence measured among populations reflects species-level differentiation remains a central challenge in species delimitation. One potential solution is to compare genetic divergence between putative new species with other closely related species, sometimes referred to as a reference-based taxonomy. To be described as a new species, a population should be at least as divergent as other species. Here, we develop a reference-based taxonomy for Horned Lizards ( Phrynosoma ; 17 species) using phylogenomic data (ddRADseq data) to provide a framework for delimiting species in the Greater Short-horned Lizard species complex ( P. hernandesi ). Previous species delimitation studies of this species complex have produced conflicting results, with morphological data suggesting that P. hernandesi consists of five species, whereas mitochondrial DNA support anywhere from 1 to 10 + species. To help address this conflict, we first estimated a time-calibrated species tree for P. hernandesi and close relatives using SNP data. These results support the paraphyly of P. hernandesi; we recommend the recognition of two species to promote a taxonomy that is consistent with species monophyly. There is strong evidence for three populations within P. hernandesi , and demographic modeling and admixture analyses suggest that these populations are not reproductively isolated, which is consistent with previous morphological analyses that suggest hybridization could be common. Finally, we characterize the population-species boundary by quantifying levels of genetic divergence for all 18 Phrynosoma species. Genetic divergence measures for western and southern populations of P. hernandesi failed to exceed those of other Phrynosoma species, but the relatively small population size estimated for the northern population causes it to appear as a relatively divergent species. These comparisons underscore the difficulties associated with putting a reference-based approach to species delimitation into practice. Nevertheless, the reference-based approach offers a promising framework for the consistent assessment of biodiversity within clades of organisms with similar life histories and ecological traits. 
    more » « less