Comparative Phylogeographic Analyses Illustrate the Complex Evolutionary History of Threatened Cloud Forests of Northern Mesoamerica

Abstract

Comparative phylogeography can elucidate the influence of historical events on current patterns of biodiversity and can identify patterns of co-vicariance among unrelated taxa that span the same geographic areas. Here we analyze temporal and spatial divergence patterns of cloud forest plant and animal species and relate them to the evolutionary history of naturally fragmented cloud forests–among the most threatened vegetation types in northern Mesoamerica. We used comparative phylogeographic analyses to identify patterns of co-vicariance in taxa that share geographic ranges across cloud forest habitats and to elucidate the influence of historical events on current patterns of biodiversity. We document temporal and spatial genetic divergence of 15 species (including seed plants, birds and rodents), and relate them to the evolutionary history of the naturally fragmented cloud forests. We used fossil-calibrated genealogies, coalescent-based divergence time inference, and estimates of gene flow to assess the permeability of putative barriers to gene flow. We also used the hierarchical Approximate Bayesian Computation (HABC) method implemented in the program msBayes to test simultaneous versus non-simultaneous divergence of the cloud forest lineages. Our results show shared phylogeographic breaks that correspond to the Isthmus of Tehuantepec, Los Tuxtlas, and the Chiapas Central Depression, with the Isthmus representing the most frequently shared break among taxa. However, dating analyses suggest that the phylogeographic breaks corresponding to the Isthmus occurred at different times in different taxa. Current divergence patterns are therefore consistent with the hypothesis of broad vicariance across the Isthmus of Tehuantepec derived from different mechanisms operating at different times. This study, coupled with existing data on divergence cloud forest species, indicates that the evolutionary history of contemporary cloud forest lineages is complex and often lineage-specific, and thus difficult to capture in a simple conservation strategy.

Historical and current introgression in a Mesoamerican hummingbird species complex: a biogeographic perspective

“…This divergence time has been reported for species/subspecies mtDNA level splits in other Mesoamerican avian groups (e.g., Barrera-Guzmán et al, 2012;Ornelas et al, 2013;Malpica & Ornelas, 2014;Rodríguez-Gómez & Ornelas, 2014), suggesting an important role of Pleistocene glacial cycles in autochthonous diversification. Given that divergence time estimates were obtained with mtDNA only (not likely to resemble the species phylogeny), divergence times might differ substantially if estimated with both mtDNA and nuDNA sequence data (McCormack, Zellemer & Knowles, 2010).…”

“…Within Mesoamerica, continuous tectonic activity uplifted the highlands and repeated cycles of forest contraction and expansion in the highlands, owing to Pleistocene climate cycles, formed a set of corridors and barriers, creating further isolation and shaping genetic divergence and autochthonous diversification in the region at different time scales (e.g., Gutiérrez-García & Vázquez-Domínguez, 2012;Rodríguez-Gómez & Ornelas, 2014;Rovito et al, 2015). Several phylogeographical studies have shown marked genetic divergence between populations on either side of the Isthmus of Tehuantepec in southern Mexico, a common barrier of dry scrubby lowlands for many taxa (e.g., Bonaccorso et al, 2008;Barber & Klicka, 2010;Barrera-Guzmán et al, 2012;Ornelas et al, 2013;Ortiz-Ramírez et al, 2016), including hummingbirds (Cortés-Rodríguez et al, 2008;González, Ornelas & Gutiérrez-Rodríguez, 2011;Arbeláez-Cortés & Navarro-Sigüenza, 2013;Rodríguez-Gómez, Gutiérrez-Rodríguez & Ornelas, 2013;Zamudio-Beltrán & Hernández-Baños, 2015;Rodríguez-Gómez & Ornelas, 2015), and between populations separated by the Nicaraguan Depression, a lowland corridor running from the Caribbean to the Pacific near the border between Costa Rica and Nicaragua (Bonaccorso et al, 2008;Zamudio-Beltrán & Hernández-Baños, 2015;Ortiz-Ramírez et al, 2016). However, these geographic barriers seem permeable for highland species during the colder stages of the glacial cycles (Gutiérrez-Rodríguez, Ornelas & Rodríguez-Gómez, 2011; W Colombia, and A. s. braccata in the Andes of W Venezuela) are currently recognized based on geography ( Fig.…”

Phylogeographic structure of Canthon cyanellus (Coleoptera: Scarabaeidae), a Neotropical dung beetle in the Mexican Transition Zone: Insights on its origin and the impacts of Pleistocene climatic fluctuations on population dynamics

“…Forests drifted to the south during the Pleistocene colder periods; then they 16 returned to the North during the warmer periods (Gómez-Pompa, 1973). This process might have promoted vicariant events as has been suggested for other taxa distributed within Mexico (Guevara-Chumacero et al, 2010;Maldonado-Sánchez et al, 2016;Ornelas et al, 2013;Suárez-Atilano et al, 2014). Finally, the discovery of four individuals collected at the gf population that are genetically more related to individuals at the NGM region than to the other gf samples provide evidence of contemporary migration.…”

“…It is likely that the microhabitat characteristics prevailing in forest fragments during the Pleistocene, during the interglacial when temperatures became warmer (Gibbard et al, 2010), would have allowed these beetles to find favorable conditions to breed. Similarly, Ornelas et al (2013), found a Pleistocene divergence between different taxa associated to cloud forests in Mexico. These authors suggest that the genetic differentiation of the study species can be explained by the forest dynamics as influenced by the Quaternary climatic fluctuations.…”

Toward a paradigm shift in comparative phylogeography driven by trait-based hypotheses

“…With concordance as a metric for testing expectations for patterns of genetic variation, comparative phylogeographic analyses have been used to address a broad array of ecological and evolutionary questions, from inferring Quaternary refugia and assigning conservation priorities (6,7) to evaluating the stability of ecological associations between interacting organisms (8,9). Commonly applied tests include the evaluation of spatially concordant phylogeographic breaks (10,11), temporally synchronous population divergence (12,13), or concerted demographic expansion/contraction (14,15) among members of an ecological community.…”