Phylogeography, Historical Population Demography, and Climatic Modeling of Two Bird Species Uncover Past Connections Between Amazonia and the Atlantic Forest

Abstract

We combined mitochondrial DNA sequence data and paleoclimatic distribution models to document phylogeographic patterns and investigate the historical demography of two manakins, Ceratopipra rubrocapilla and Pseudopipra pipra, as well as to explore connections between Amazonia and the Atlantic Forest. ND2 sequences of C. rubrocapilla (75 individuals, 24 sites) and P. pipra (196, 77) were used in Bayesian inference and maximum likelihood analyses. We estimated mitochondrial nucleotide diversity, employed statistical tests to detect deviations from neutral evolution and constant population sizes, and used species distribution modeling to infer the location of suitable climate for both species under present-day conditions, the Last Glacial Maximum (LGM), and the Last Interglacial Maximum (LIG). Mitochondrial sequence data from C. rubrocapilla indicate one Amazonian and one Atlantic Forest haplogroup. In P. pipra, we recovered a highly supported and differentiated Atlantic Forest haplogroup embedded within a large Southern Amazonian clade. Genetic and taxonomic structure in Amazonia differs widely between these two species; older P. pipra has a more marked genetic structure and taxonomic differentiation relative to the younger C. rubrocapilla. Both species have similar genetic patterns in the Atlantic Forest. Paleoclimatic distribution models suggest connections between southwestern Amazonia and the southern Atlantic Forest during the LIG, but not between eastern Amazonia and the northeastern Atlantic Forest, as suggested by previous studies. This indicates that multiple corridors, and at different locations, may have been available over the Pliocene and Pleistocene between these two regions.

Keywords: Atlantic Forest; Ceratopipra rubrocapilla; Pseudopipra pipra; historical demography; mitochondrial DNA; phylogeography; species distribution modeling.

FIGURE 1

(a) Bayesian Inference of Ceratopipra rubrocapilla based on 1041 bp of the ND2 gene. Numbers correspond to posterior probabilities and Maximum Likelihood bootstraps. Ceratopipra chloromeros, C. erythrocephala , C. mentalis , and Machaeropterus deliciosus were used as outgroups (not shown). (b) Map showing current distribution of C. rubrocapilla and sampling localities included in the molecular analyses. Haplotypes are color‐coded according to localities, as shown on the map. (c) Median joining network showing all samples of C. rubrocapilla (1041 bp of ND2, n = 75 sequences). Each circle represents a haplotype, and the size of the circle is proportional to the number of individuals having that haplotype.

FIGURE 2

(a) Bayesian Inference of Pseudopipra pipra based on 1041 bp of the ND2 gene. Numbers correspond to posterior probabilities and Maximum Likelihood bootstraps. Ceratopipra rubrocapilla, Heterocercus linteatus , and Machaeropterus deliciosus were used as outgroups (not shown). (b) Map showing current distribution of P. pipra and sampling localities included in the molecular analyses. Haplotypes are color‐coded according to localities from different regions throughout the distribution, as shown on the map. (c) Median joining network showing all samples of P. pipra (above, 1041 bp of ND2, n = 196 sequences). Each circle represents a haplotype, and the size of the circle is proportional to the number of individuals having that haplotype.

FIGURE 3

Bayesian Inference‐based divergence times of Ceratopipra rubrocapilla and Pseudopipra pipra, based on 1041 bp of the ND2 gene. Manacus manacus , Heterocercus linteatus , Lepidothrix coronata , Machaeropterus deliciosus , Ceratopipra cornuta, C. mentalis , C. erythrocephala , and C. chloromeros were used as outgroups (the first three outgroups are not showing in the tree). Numbers below the line indicate node posterior probabilities ≥ 0.5, with the * representing ≥ 0.95 posterior probability. Blue bars on nodes correspond to the 95% highest posterior density (HPD) intervals of the time estimates. For relevant nodes, numbers above the line indicate median values and 95% posterior age intervals in million years.

FIGURE 4

Demographic history of Ceratopipra rubrocapilla inferred through extended Bayesian skyline plots (EBSPs) estimated in BEAST, based on ND2 sequence data. Dashed lines depict median population size, area in gray denotes 95% Bayesian Credible Intervals. Time scale in millions of years before present.

FIGURE 5

Demographic history of Pseudopipra pipra lineages inferred through extended Bayesian skyline plots (EBSPs) estimated in BEAST, based on ND2 sequence data. Dashed lines depict median population size, area in gray denotes 95% Bayesian Credible Intervals. Time scale in millions of years before present.

FIGURE 6

Modeled suitable climatic conditions for Ceratopipra rubrocapilla and Pseudopipra pipra across Quaternary climatic fluctuations, and current climate. Green color indicates low predicted suitability, yellow to red colors indicate higher values, and white areas indicate those pixels with values below the minimum training presence (MTP) threshold, as determined based on the calibration data. Dots on the current climate map depict localities of known species occurrence; dots on the Atlantic Forest region indicate localities for which genetic data were collected (LGM, last glacial maximum; LIG, last interglacial maximum).