Date Published: March 20, 2019
Publisher: Public Library of Science
Author(s): Cássia Alves Lima-Rezende, Amanda Vaz Rocha, Antônio Felipe Couto Júnior, Éder de Souza Martins, Vinicius Vasconcelos, Renato Caparroz, Łukasz Kajtoch.
We performed phylogeographic and genetic structure analyses of Neothraupis fasciata joined with species distribution modelling to evaluate whether: (1) the distribution of genetic variability shows a pattern expected by the isolation-by-distance model; (2) the influence of the Pleistocene climate changes on species distribution; and (3) climate/climatic stability (hypothesis of climatic stability) as a predictor of population genetic diversity. Based on two molecular datasets (ND2 and FIB-5), the isolation-by-distance hypothesis was not supported. The mitochondrial haplotype network indicated the existence of historically isolated populations at the southern range of the species distribution, and recent population expansion was identified by both neutrality tests and extended Bayesian skyline plot analysis. Thus, the climatic changes during the Pleistocene might have promoted the reconnection of the partially isolated southern populations, which may have persisted in the plateaus during the cycles of savanna contractions. Subsequently, this species (re)colonized northern areas of the species present distribution, following the continuous vegetation on the São Francisco and Central plateaus about 60 kyr, and also reached the Amazonian savannas likely via the central corridor. Thus, our results indicated that the intrinsic relationship between the relief heterogeneity (plateaus and depressions) and the climatic fluctuations, mainly in the Pleistocene, promoted population reconnection and demographic expansion of N. fasciata.
Tertiary geological events and the Quaternary climatic changes have been considered the key events related to the biodiversity diversification (e.g. [1–5]). Specifically, the Quaternary climatic cycles had great importance in South American forest and nonforest vegetation (e.g. Savannas) range dynamics [1,3,6–12]. Briefly, it is postulated that during moist and warm periods (interglacial periods), forests expanded their ranges, while during the cold and dry periods (glacial periods) the savannas reached their maximum extension (see ). Events of both range contraction and expansion during glacial periods have been hypothesized for the “morphoclimatic domain of the Cerrado” [13,14], hereafter referred to as the Cerrado. For instance, during the glacial period the current range of this savanna was replaced by Araucaria forests at its southern edge and by xeric forests at its northern edge, while it was expanded throughout eastern and central Amazonia . According to Werneck et al. , during the Last Interglacial (LIG, c. 120,000 years ago or 120 kyr) the Cerrado expanded, while during the Last Glacial Maximum (LGM, c. 21 kyr) the Cerrado reached its smallest range. It is also postulated that during the Pleistocene the forest and nonforest vegetation range dynamics may have led to the establishment of biogeographic corridors currently connecting the isolated savanna blocks in northern Amazonia Forest (Llanos and Amazonian savannas) and Cerrado [1,9,15–20]. The dynamic of range shifts of the Cerrado is complex and there is still no clear pattern related to the diversification of the Cerrado biodiversity that has emerged driven by Pleistocene climatic fluctuations. Considering that the Cerrado is one of the biodiversity hotspots [21–23], understanding the processes that led to the diversification of its biodiversity is also fundamental for its conservation.
In the present study, we assessed the levels of genetic diversity and structure in Neothraupis fasciata based on samples from a wide geographic area in the Cerrado. Our data support a single population (supported by BAPS results) with a weak genetic structure (global ΦST), in which southernmost locations showed more genetic variability than those sampled in the northern Cerrado. Considering that areas of greater genetic diversity are commonly associated with the origin center of a species (e.g. [25,27,76]), it is plausible to assume that the origin center of the N. fasciata lineage is in the southern part of the Cerrado. The southern Cerrado encompasses some topographical relief core areas, such as Parecis, Paraná-Guimarães and Serra da Canastra plateaus, which are, at least in part, concordant with some predicted stable areas (see Fig 3). These historically stable areas may have played an important role in the speciation process and also served as refugia favoring higher levels of genetic diversity for this species. Additionally, according to the phylogeny of the Thraupidae family , the distribution range of the N. fasciata sister species (Lophospingus pusillus, Lophospingus griseocristatus, Gubernatrix cristata, and Diuca diuca) is restricted to southern South America .
Genetic groups of N. fasciata located in the southern part of the species distribution (likely its center of origin) might have persisted in partially isolated populations restricted to the plateaus during the cycles of savanna contractions. Subsequent events of savanna expansion promoted the reestablishment of gene flow among these isolated populations and the increase in the distribution range through the (re)colonization of the northern portion of the species distribution. Thus, the intrinsic relationship between the relief heterogeneity (plateaus and depressions) and the climatic fluctuations, mainly in the Pleistocene, promoted population reconnection and demographic expansion of N. fasciata, reinforcing previous studies (e.g. ) that suggest that this relation of cause and effect (the interaction between climate and relief defining vegetation dynamic) may have been decisive in the diversification of the Cerrado biodiversity.