Synthesis of geological and comparative phylogeographic data point to climate, not mountain uplift, as driver of divergence across the Eastern Andean Cordillera

Abstract

AimTo evaluate the potential role of the orogeny of the Eastern Cordillera (EC) of the Colombian Andes and the Mérida Andes (MA) of Venezuela as drivers of vicariance between populations of 37 tetrapod lineages co-distributed on both flanks, through geological reconstruction and comparative phylogeographic analyses.LocationNorthwestern South AmericaMethodsWe first reviewed and synthesized published geological data on the timing of uplift for the EC-MA. We then combined newly generated mitochondrial DNA sequence data with published datasets to create a comparative phylogeographic dataset for 37 independent tetrapod lineages. We reconstructed time-calibrated molecular phylogenies for each lineage under Bayesian inference to estimate divergence times between lineages located East and West of the Andes. We performed a comparative phylogeographic analysis of all lineages within each class of tetrapod using hierarchical approximate Bayesian computation (hABC) to test for synchronous vicariance across the EC-MA. To evaluate the potential role of life history in explaining variation in divergence times among lineages, we evaluated 13 general linear models (GLM) containing up to six variables each (maximum elevation, range size, body length, thermoregulation, type of dispersal, and taxonomic class).ResultsOur synthesis of geological evidence suggested that the EC-MA reached significant heights by 38–33 million years ago (Ma) along most of its length, and we reject the oft-cited date of 2–5 Ma. Based on mtDNA divergence from 37 lineages, however, the median estimated divergence time across the EC-MA was 3.26 Ma (SE = 2.84) in amphibians, 2.58 Ma (SE = 1.81) in birds, 2.99 Ma (SE = 4.68) in reptiles and 1.43 Ma (SE = 1.23) in mammals. Using Bayes Factors, the hypothesis for a single temporal divergence interval containing synchronous divergence events was supported for mammals and but not supported for amphibians, non-avian reptiles, or birds. Among the six life-history variables tested, only thermoregulation successfully explained variation in divergence times (minimum AICc, R2 0.10), with homeotherms showing more recent divergence relative to poikilotherms.Main conclusionsOur results reject the hypothesis of the rise Andean Cordillera as driver of vicariance of lowland population because divergence dates are too recent and too asynchronous. We discuss alternative explanations, including dispersal through mountain passes, and suggest that changes in the climatic conditions during the Pliocene and Pleistocene interacted with tetrapod physiology, promoting older divergences in amphibians and reptiles relative to mammals and birds on an already established orogen.

Landscape Genetics and Species Delimitation in the Andean Palm Rocket Frog (Aromobatidae, Rheobates)

“…This is mostly due to the rain shadow effect caused by the trade winds that come from the east [71]. In this case, the geographic variation in environment, i.e., higher humidity along the eastern slope relative to the western slope, is due to a potential geographic barrier, the Eastern Cordillera (but see [16]). Assuming uniformitarianism that the same processes have been acting on Rheobates across its 35 million year history (the estimated stem age reported by Muñoz-Ortiz et al [32]), a potential scenario would be that initial divergences are driven by local adaptation to environmental variation while obvious landscape features may arise secondarily, such as through the formation of valleys or mountain peaks.…”

“…The Andean uplift created valleys that may have promoted the diversification of a variety of organisms, for example, the wax palm genus Ceroxylon [10], the Ithomiini tribe of butterflies [11,12], the montane forest subspecies of the three-striped warbler bird, suggested to have occured by allopatric divergence [13], and the Adelomyia hummingbirds, whose divergence was coupled to Andean orogeny [14]. The rise of Andean peaks promoted lowland speciation in some groups, such as the Dendrocincla woodcreepers, through vicariance during the uplift [15], yet many lowland tetrapods appear to have been largely unaffected by Andean vicariance [16].…”

Landscape genetics and species delimitation in the Andean palm rocket frog,Rheobatesspp

“…This is mostly due to the rain shadow effect caused by the trade winds that come from the east (Mark & Helmens, 2005). In this case the geographic variation in environment, i.e., higher humidity along the eastern slope relative to the western slope, is due to a potential geographic barrier, i.e., the Eastern Cordillera (but see Rodríguez-Muñoz et al, 2020). Assuming uniformitarianism, that the same processes have been acting on Rheobates across its 35 million year history [the estimated stem age reported by Muñoz-Ortiz et al (2015)], a potential scenario would be that initial divergences are driven by local adaptation to environmental variation while obvious landscape features may arise secondarily, such as through the formation of valleys or mountain peaks that secondarily act as barriers.…”

“…Even though some studies suggest that the Andean topography promotes genetic divergence and diversification in the tropics (Chaves et al, 2011;Gutiérrez-Pinto et al, 2012;Weir & Price, 2011), further investigation is needed to understand the origins of this diversity. In a recent pre-print, Rodríguez-Muñoz et al(2020) suggested that environment, rather than Andean uplift is the main factor explaining genetic divergence across lowland tetrapod species separated by the Eastern Andes. However, when invoking environment as a barrier, there are two factors to consider: one is the more typical assumption that the environment of the intervening region is what isolates pairs of populations, while the second possibility is the distinctiveness of the environment that characterizes the respective populations.…”

Andean uplift, drainage basin formation, and the evolution of riverweeds(Marathrum,Podostemaceae)in northern South America

“…4.5 Ma, resulting in the current elevation of the Andes (Gregory-Woodzicki, 2000; Garzione et al , 2008; Mora et al , 2010; Hoorn et al , 2010). These dates are contested by geological studies of mainly coarse-grained deposits that suggest that the Eastern Cordillera was already well underway in Eocene times and nearly complete in the Late Miocene (>11 Ma) (Cooper et al , 1995; Montes et al , 2019; Rodríguez-Muñoz et al , 2020). Our divergence dating analysis results in Fig.…”