Extreme genetic structure and dynamic range evolution in a montane passerine bird: implications for tropical diversification

Abstract

17Aim: Employ phylogeographic analyses of a widespread species complex to examine the role of historical and 18 evolutionary processes in the origin and maintenance of high species diversity in the Neotropical montane region. 19 20Location: Neotropical highlands. 21 22Taxon: Henicorhina wood-wrens (Aves, Troglodytidae). 23 24Methods: We collected mtDNA sequence data for 288 individuals thoroughly covering the range of the Henicorhina 25 leucophrys complex from Mexico to Bolivia. Sequences were employed to characterize population structure, infer 26 phylogenetic relationships among populations and their divergence times, examine lineage accumulation through time, 27and identify presumptive species using coalescent methods. We also explored the origin of elevational and latitudinal 28replacements involved in spatial changes in species assemblages in the Andes. 29 30Results: We found remarkable genetic structure within the complex, which consists of numerous lineages reaching 31 >12% sequence divergence; most divergent populations occur in areas separated by topographic barriers but several of 32 them, typically not sister to each other, co-occur with elevational segregation on mountain slopes or replace each other 33with latitude along the Andes. Some close relatives occur in areas separated by thousands of kilometers, with more 34 distant relatives occupying intervening areas. The complex likely originated in the Mexican highlands and expanded 35 extensively in South America while diverging rapidly at a constant rate into many different lineages which have 36 persisted for millions of years. Coalescent analyses consistently revealed that the complex may comprise more than 30 37 species; while we do not suggest these presumptive species should be recognized by taxonomists in the absence of 38 additional data, H. leucophrys is a distant outlier among New World birds in terms of high lineage diversity within a 39 single recognized species. 40 41Main Conclusions: Our study captured wood-wren lineages in the act of building up diversity via divergence and 42 persistence in allopatry, achievement of secondary sympatry, and coexistence at the landscape scale mediated by 43 ecological and evolutionary divergence. Although dispersal by wood-wrens is restricted at present and this likely 44 accounts for strong population structure across topographic barriers, their ranges have been dynamic, managing to 45 disperse over much of the montane Neotropics. Phases of expansion and contraction of ranges and localized extinctions 46 of populations likely account for phylogeographic patterns which are precursors to the origin of new species and the 47 accumulation of diversity in tropical mountains. 48 49

Rugged relief and climate promote isolation and divergence between two neotropical cold‐associated birds

“…The strong population structure found here (Fig. 2B) is consistent with the observed patterns in other Neotropical montane systems (e.g., Andes), where diversification was likely a consequence of allopatric isolation in response to complex topography and cyclic climatic changes (Perez-Eman, 2005;Gutiérrez-Pinto et al, 2012;Valderrama et al, 2014;Winger and Bates, 2015;Cadena et al, 2019). However, the lineages recovered in our study and their recent origin contradict previous studies on other organisms ranging broadly in MAF, the latter which did not recover obvious phylogeographic breaks (e.g., Batalha-Filho et al, 2012;Peres et al, 2015) or recovered much older splits (e.g., Pulido-Santacruz et al, 2016, Pie et al, 2018Peres et al, 2018;.…”

“…In these regions, the historical fragmentation and contraction of habitats and subsequent dispersal mediated by rugged relief and climate fluctuations are thought to be key factors underlying the dynamics of diversification (Mayr and Diamond, 1976;Patton and Smith, 1992;Graham et al, 2014;Antonelli, 2015;Rangel et al, 2018). While empirical evidence addressing the interplay between climate and topography has been available for some time and has provided invaluable insights into the diversification of tropical montane organisms ( Van der Hammen, 1961;Hooghiemstra and Van der Hammen, 2004;Chesser, 2000;Pérez-Emán, 2005;Bonaccorso, 2009;Weir, 2009;Gutiérrez-Pinto et al, 2012;Ramírez-Barahona and Eguiarte, 2013;Valderrama et al, 2014;Winger and Bates, 2015;Manthey et al 2017, Cadena et al, 2019, Muellner-Riehl 2019, Rahbek et al, 2019, our ability to understand these range shifts in the recent and more distant past and the genomic footprint left by them is still limited. This is because these processes have rarely been empirically investigated in a detailed explicit spatiotemporal framework.…”

Molecular and morphological differentiation among Torrent Duck (Merganetta armata) populations in the Andes

“…The observed pattern of relatively rapid divergence among well‐differentiated groups, which does not allow to clearly disentangle their relationships, has also been recovered in several codistributed species occupying forest habitats (Cadena, ; Cadena et al, , ; Chaves & Smith, ; Gutiérrez‐Pinto et al, ; Isler, Cuervo, Bravo, & Brumfield, ; Pérez‐Emán, ; Weir et al, ). The presence of such seemingly common patterns in phylogeographic studies of Andean birds suggests that bird assemblages, including species occupying different habitats, may have been affected by features of the landscape and climatic or tectonic changes in similar ways.…”

Genetic, vocal, and body size divergence across the Northern Peruvian Low supports two species within the Masked Flowerpiercer (Diglossa cyanea)

“…For instance, marked phenotypic differences exist between recently diverged, almost genetically indistinguishable populations of Coeligena hummingbirds (Palacios et al 2019). On the other hand, phenotypically indistinguishable populations with deep genetic divergences are found in several Andean bird complexes, including ducks (Gutiérrez-Pinto et al 2019), hummingbirds (Chaves et al 2011, Benham et al 2014), suboscines (Valderrama et al 2014, Cadena et al 2020), and oscines (Gutiérrez-Pinto et al 2012, Prieto-Torres et al 2018, Cadena et al 2019). That is, true diversity may be frequently overlooked due to characterizations based on genetic or phenotypic traits alone.…”