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Tuesday, 14 October 2014

Speciation in Tropical Bird Populations: Large-scale geographical transformation barriers or dispersal and differentiation? Smith et al, Nature September 2014.

The drivers of tropical speciation.

Nature. 2014 Sep 10. doi: 10.1038/nature13687. [Epub ahead of print]
PMID: 25209666 [PubMed - as supplied by publisher]



Smith BT, McCormack JE, Cuervo AM, Hickerson MJ, Aleixo A, Cadena CD, Pérez-Emán J, Burney CW, Xie X, Harvey MG, Faircloth BC, Glenn TC, Derryberry EP, Prejean J, Fields S, Brumfield RT.

These authors contributed equally to this work.
Brian Tilston Smith & Robb T. Brumfield


Museum of Natural Science, Louisiana State University, Baton Rouge, Louisiana 70803, USA

Since the recognition that allopatric speciation can be induced by large-scale reconfigurations of the landscape that isolate formerly continuous populations, such as the separation of continents by plate tectonics, the uplift of mountains or the formation of large rivers, landscape change has been viewed as a primary driver of biological diversification. This process is referred to in biogeography as vicariance. In the most species-rich region of the world, the Neotropics, the sundering of populations associated with the Andean uplift is ascribed this principal role in speciation. An alternative model posits that rather than being directly linked to landscape change, allopatric speciation is initiated to a greater extent by dispersal events, with the principal drivers of speciation being organism-specific abilities to persist and disperse in the landscape. Landscape change is not a necessity for speciation in this model. Here we show that spatial and temporal patterns of genetic differentiation in Neotropical birds are highly discordant across lineages and are not reconcilable with a model linking speciation solely to landscape change. Instead, the strongest predictors of speciation are the amount of time a lineage has persisted in the landscape and the ability of birds to move through the landscape matrix. These results, augmented by the observation that most species-level diversity originated after episodes of major Andean uplift in the Neogene period, suggest that dispersal and differentiation on a matrix previously shaped by large-scale landscape events was a major driver of avian speciation in lowland Neotropical rainforests.

Figure 1
Sampling points of the 27 bird lineages (circles) and prominent dispersal barriers within the landscape matrix, including the Andes (and associated arid habitats in the Caribbean lowlands of South America), the Isthmus of Panama and three major rivers in the Amazon Basin (Amazon, Negro and Madeira Rivers).

Figure 2
An exemplar taxon for each lineage is illustrated. Yellow bars correspond to the 95% highest posterior density for divergence times of each species. The Quaternary (2.6 Myr ago–present) and the Neogene (23–2.6 Myr ago) periods are shaded in grey and light blue, respectively. Mean stem ages for 25 of the lineages occurred within the Neogene and for two lineages within the Quaternary. Outgroups for each lineage are not included in the depicted phylogeny.

Figure 3
a, The variation in divergence times across barriers cannot be attributed to ecologically mediated vicariance. There was no significant association between dispersal ability and divergence times across the Andes and the Isthmus of Panama. Only part of the variance in divergence times across rivers was attributable to dispersal ability. Divergence levels across Amazonian rivers were generally shallower in canopy birds, but understorey birds diverged multiple times across each river. Circles represent mean estimates and bars represent the 95% highest posterior density. Colour coding of the points corresponds to the foraging stratum of each lineage: understorey, orange; canopy, green. Vertical hashed lines at 2.58 million years represent the transition between the Neogene (to the right of line) and Quaternary (to the left of line). b, Within-lineage species diversity increases with lineage (stem) age. Solid lines represent the fit of the data to a model using phylogenetic generalized least-squares analyses. Black points and line correspond to mean stem ages, and the purple points and lines correspond to the high and low values of the stem age 95% highest posterior density. c, Box plot illustrating that species diversity is significantly higher in the understorey lineages than in forest canopy lineages. The box plot shows the first, second and third quartiles, the lines are the 95% confidence intervals and the circles represent outliers. Significant associations in panels a, b and c are supported by phylogenetic generalized least-squares analyses shown in Table 1 and Supplementary Tables 9–15. Statistical tests were performed independently on each data set except for divergences across rivers; all rivers were combined into a single analysis.

The accumulation of bird species in the Neotropical landscape occurred through a repeated process of geographical isolation, speciation, and expansion, with the amount of species diversity within lineages influenced by how long the lineage has persisted in the landscape and its ability to disperse through the landscape matrix. A growing body of phylogenetic evidence indicates that average rates of avian diversification have been relatively constant in the Neotropics and, consistent with this, our results show that tumultuous changes to the South American landscape may not have led to marked pulses in speciation. Correlations between lineage ages and the Andean uplift or Quaternary climatic events reported elsewhere are suggestive of landscape and environmental change being a component of the diversification process, but the details of how, when and to what extent these changes drove the origin of standing species-level diversity remain unclear. Our phylogeographic-scale analysis indicated most species-level variation postdates the Andean uplift, and our results contribute to a growing number of studies reporting dispersal events as the primary initiators of geographical isolation and speciation. Our results also have an important conservation implication. Anthropogenic alterations of the landscape matrix by deforestation and climate change affect not only the evolutionary persistence of rainforest lineages, but also the occurrence of cross-barrier dispersal events within lineages that lead to new biological diversity.

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