Underlying microevolutionary processes parallel macroevolutionary patterns in ancient neotropical mountains

Abstract

Aim: Ancient climatic fluctuations are invoked as the main driving force that generates the astonishing biodiversity in ancient mountains. As a result, endemism and spatial turnover are usually high and few species are widespread amongst entire mountain ranges, precluding the understanding of origins of macroevolutionary patterns. Here, we used a species endemic to, but widespread in, one of the most species-rich ancient mountains in the globe to test how environmental changes acted on and how their macroevolutionary patterns were shaped.Location: Espinhaço Range, Eastern Brazil. Taxon: Vriesea oligantha species complex (Bromeliaceae). Methods:We compiled data for plastidial regions and nuclear microsatellites to assess genetic diversity, population structure, migration rates and phylogenetic relationships. Using temperature and precipitation variables, we modelled suitable areas for the present and the past, estimating corridors between isolated populations. We also implemented Bayesian demographic analyses to estimate ancient populations dynamics. Finally, we tested if population structure is driven by isolation by environment or by distance using a Bayesian modelling approach.Results: Our results showed that the intraspecific divergence events of V. oligantha are older than those associated with the latest Pleistocene climatic oscillations, supporting the view that Quaternary climatic fluctuations are key components for understanding its population differentiation processes. Species distribution modelling estimated corridors between populations in the past, as also shown in the demographic analyses, depicting a major spatial reorganization during colder climates.Besides, the high genetic structure estimated results from both models of isolation by distance and by environment. Main conclusions: V. oligantha is a remarkable model to test the effects of climatic oscillations over the biological community, since this species originated in the early-Pleistocene, prevailing over several cycles of climatic fluctuations until today. The estimated demographic dynamics of V. oligantha agrees with the species-pump mechanism, suggesting it as the main cause of speciation within the Espinhaço Range. Moreover, the phylogeographic patterns of V. oligantha reflect previously recognised | 2313 DANTAS-QUEIROZ ET Al.

Comparative phylogeography reveals the demographic patterns of neotropical ancient mountain species

“…The congruence between intraspecific lineages and biogeographic patterns for the Espinhaço Range was firstly noted for the bromeliad Stigmatodon oliganthus (Dantas‐Queiroz et al, 2021). In that study, the authors explicit this fact showing that the congruence between the microevolutionary patterns of S. oliganthus and the macroevolutionary patterns of the Espinhaço is a consequence of common drivers found among those mountains, such as ancient climatic oscillations.…”

“…Differently from the effects of the LGM on high latitude areas of the globe, climatic oscillations from this period did not provide extreme events such as the formation of glacial sheets or mountaintops freezing on Eastern South America, phasing out a “tabula rasa” scenario (i.e., completely wiping out the biota on these mountains) (Chaves et al, 2004; Pfanzelt et al, 2017). On the contrary, pulses of connectivity and contraction over the Pleistocene allowed a complex evolutionary arena of isolation, secondary contact, and hybridization (Antonelli et al, 2010; Dantas‐Queiroz et al, 2021; Ribeiro et al, 2014). In consequence, prior climatic oscillations might have promoted divergence and spatial structure on BQM (Ribeiro et al, 2014; Vasconcelos et al, 2020).…”

“…Due to the intrinsic nature of endemic species, few taxa are widely distributed along the BQM, hampering a broad genetic spatial comparison among species from the same region (Dantas‐Queiroz et al, 2021). Nonetheless, the Espinhaço Range is one of the main BQM areas, where biogeographic regionalization areas (bioregions hereafter) have been proposed mainly based on plant endemism (Campos et al, 2019; Colli‐Silva et al, 2019; Echternacht et al, 2011).…”

“…Nonetheless, the Espinhaço Range is one of the main BQM areas, where biogeographic regionalization areas (bioregions hereafter) have been proposed mainly based on plant endemism (Campos et al, 2019; Colli‐Silva et al, 2019; Echternacht et al, 2011). Thus, to test for congruent phylogeographic patterns in the Espinhaço Range, we selected four species that occur along these mountains, two eudicots, Richterago discoidea (Asteraceae) (Barres et al, 2019) and Euphorbia attastoma (Euphorbiaceae) and two monocots, Neoregelia bahiana and Stigmatodon oliganthus (= Vriesea oligantha ) (Bromeliaceae) (Couto et al, 2022; Dantas‐Queiroz et al, 2021). The phylogeographic congruency between species were tested using the phylogeographic concordance factors (PCFs), an index developed by Satler and Carstens (2016).…”

Ten principles for restoring campo rupestre, a threatened tropical, megadiverse, nutrient‐impoverished montane grassland

“…However, this is rarely the case for campo rupestre . Studies generally report extremely low between‐population seed flow in campo rupestre regardless of climatic variations (Fiorini et al 2019; Dantas‐Queiroz et al 2021), while others support Pleistocene climatic variation‐mediated dispersal and isolation (Barres et al 2019). Past demography processes are determinants for genetic structure and adaptative potential, thus when lacking genetic data, seed sourcing should consider the risk of both endogamic and exogamic depressions (Gann et al 2019).…”