Comparative phylogeography reveals the demographic patterns of neotropical ancient mountain species

Abstract

Mountains are renowned for their bountiful biodiversity. Explanations on the origin of such abundant life are usually regarded to their orogenic history. However, ancient mountain systems with geological stability also exhibit astounding levels of number of species and endemism, as illustrated by the Brazilian Quartzitic Mountains (BQM) in Eastern South America. Thus, cycles of climatic changes over the last couple million years are usually assumed to play an important role in the origin of mountainous biota. These climatic oscillations potentially isolated and reconnected adjacent populations, a phenomenon known as flickering connectivity, accelerating speciation events due to range fragmentation, dispersion, secondary contact, and hybridization. To evaluate the role of the climatic fluctuations on the diversification of the BQM biota, we estimated the ancient demography of distinct endemic species of animals and plants using hierarchical approximate Bayesian computation analysis and Ecological Niche Modelling. Additionally, we evaluated if climatic oscillations have driven a genetic spatial congruence in the genetic structure of codistributed species from the Espinhaço Range, one of the main BQM areas. Our results show that the majority of plant lineages underwent a synchronous expansion over the Last Glacial Maximum (LGM, c. 21 thousand years ago), although we could not obtain a clear demographic pattern for the animal lineages. We also obtained a signal of a congruent phylogeographic break between lineages endemic to the Espinhaço Range, suggesting how ancient climatic oscillations might have driven the evolutionary history of the Espinhaço's biota.

Alpine Extremophytes in Evolutionary Turmoil: Complex Diversification Patterns and Demographic Responses of a Halophilic Grass in a Central Asian Biodiversity Hotspot

“…The interglacial contraction hypothesis (or glacial expansion hypothesis) postulates that cold-adapted species demonstrated larger distribution ranges during colder periods by spreading across ice-free peripheral or lowland regions. During warmer periods these species tend to retreat to interglacial refugia towards higher latitudes or mountain summits ( Stewart et al 2010 ; Flantua et al 2019 ; Vintsek et al 2022 ; Dantas‐Queiroz et al 2023 ; Nobis et al 2023 ). This hypothesis suggests that warming could generally threaten the alpine species by aggravating habitat loss and shifting climate conditions beyond the ecological capacity of the cold-adapted organism ( Parmesan 2006 ).…”

“…The observed regional greening effect and vegetation transformations across the Asian plateaus suggest ongoing distribution shifts of plant species in this largely diverse and often harsh ecosystem ( Teng et al 2021 ; Lou et al 2023 ). Particularly, extreme climate conditions, complex geomorphic processes, and intrinsic species ecological traits are among numerous factors which could strongly affect species dispersion towards and across mountain regions ( Wang et al 2006 ; Macias-Fauria and Johnson 2013 ; Alexander et al 2018 ; Rull and Vegas-Vilarrúbia 2020 ; Na et al 2021 ; Carnicero et al 2022 ; Dantas-Queiroz et al 2023 ). Moreover, the unprecedented speed of current climate changes could pose a serious threat to highly specialized alpine organisms, hindering potential adaptive readjustments and limiting range shift opportunities ( Wiens and Graham 2005 ; Dullinger et al 2012 ; Corlett and Westcott 2013 ; Moritz and Agudo 2013 ).…”

Cryptic diversity and rampant hybridization in annual gentians on the Qinghai-Tibet Plateau revealed by population genomic analysis

“…Because the Bayankala Mountains separate populations into two genetic clusters, any observed hybridization here would likely be caused by secondary contact following range changes induced by climate oscillations. Climate oscillations cause variable connectivity across sky-islands in mountain systems as demonstrated, for example, in the HM ( Deng et al., 2020 ) and Flickering Connectivity System (Andes; Flantua et al., 2019 ; Dantas-Queiroz et al., 2023 ). In a number of cases, connectivity in the QTP region has been shown to facilitate hybridization across different genetic groups at intra- and inter-species levels ( Liu et al., 2014 ; Wu et al., 2022 ).…”

Geoclimatic drivers of diversification in the largest arid and semi‐arid environment of the Neotropics: Perspectives from phylogeography

“…Highest rates of diversification in the sky islands are timed to the Pleistocene, though major endemic lineages mostly originate in the Miocene (Carvalho et al., 2021; Inglis & Cavalcanti, 2018; Ribeiro et al., 2014; Vasconcelos et al., 2020). Pleistocene climatic fluctuations likely favoured dispersal and isolation events within and between these isolated patches, shaping the demographic histories of endemic campos rupestres species (Barres et al., 2019; Collevatti, de Castro, et al., 2012; Dantas‐Queiroz et al., 2021, 2023; Oliveira et al., 2021). In general, Pleistocene climatic fluctuations induced population expansion in campos rupestres taxa due to climatic cooling as forests retracted to lower altitudes.…”

“…During wetter and warmer interglacial periods, forests expanded to higher altitudes, isolating campos rupestres at higher elevations. Consequently, the effects of genetic drift on small and disjunctly distributed populations during periods of isolation would promote the diversification of many endemic lineages restricted to single mountaintops, as observed in frogs (Nascimento et al., 2018; Oliveira et al., 2021; Oswald et al., 2022) and plants (Dantas‐Queiroz et al., 2023; Silva et al., 2020). Many DD taxa are descended from common ancestors that diversified within the campos rupestres (likely in the Miocene), rendering the Serra do Espinhaço an ancient cradle of biodiversity.…”