Habitat shifts in the evolutionary history of a Neotropical flycatcher lineage from forest and open landscapes

Abstract

Background: Little is known about the role ecological shifts play in the evolution of Neotropical radiations that have colonized a variety of environments. We here examine habitat shifts in the evolutionary history of Elaenia flycatchers, a Neotropical bird lineage that lives in a range of forest and open habitats. We evaluate phylogenetic relationships within the genus based on mitochondrial and nuclear DNA sequence data, and then employ parsimony-based and Bayesian methods to reconstruct preferences for a number of habitat types and migratory behaviour throughout the evolutionary history of the genus. Using a molecular clock approach, we date the most important habitat shifts.

Results: Our analyses resolve phylogenetic relationships among Elaenia species and confirm several species associations predicted by morphology while furnishing support for other taxon placements that are in conflict with traditional classification, such as the elevation of various Elaenia taxa to species level. While savannah specialism is restricted to one basal clade within the genus, montane forest was invaded from open habitat only on a limited number of occasions. Riparian growth may have been favoured early on in the evolution of the main Elaenia clade and subsequently been deserted on several occasions. Austral long-distance migratory behaviour evolved on several occasions.

Conclusion: Ancestral reconstructions of habitat preferences reveal pronounced differences not only in the timing of the emergence of certain habitat preferences, but also in the frequency of habitat shifts. The early origin of savannah specialism in Elaenia highlights the importance of this habitat in Neotropical Pliocene and late Miocene biogeography. While forest in old mountain ranges such as the Tepuis and the Brazilian Shield was colonized early on, the most important colonization event of montane forest was in conjunction with Pliocene Andean uplift. Riparian habitats may have played an important role in facilitating habitat shifts by birds expanding up the mountains along streams and adapting to newly emerging montane forest habitat.

Figure 1

Distribution maps for all species-level lineages in the genus Elaenia.

Figure 2

Bayesian tree of the ND2 partition; numbers at nodes indicate parsimony bootstrap (BS; left) and Bayesian posterior probability (PP; multiplied by 100; right) values; bold numbers indicate equal support by both types of analysis; only values of BS > 60 and PP > 60 are shown.

Figure 3

Bayesian tree of the concatenated dataset; numbers at nodes indicate parsimony bootstrap (BS; left) and Bayesian posterior probability (PP; multiplied by 100; right) values; bold numbers indicate equal support by both types of analysis; only values of BS > 50 and PP > 80 are shown; thick branches additionally received high support in Fib5 analyses (BS > 80; PP = 100, except for the node uniting all three E. [o.] obscura, which only received a PP = 96); numbered cross-bars at nodes refer to parsimony-informative Fib5 indels mapped onto tree: 1.) 10-bp insertion, 2.) 1-bp deletion, 3.) 1-bp insertion, 4.) 1-bp deletion.

Figure 4

Occurrence in forest interior, natural savannah/cerrado and riparian habitats mapped onto the Elaenia tree topology derived from concatenated dataset with species-level lineages reduced to one representative; species occurring in forest interior are printed bold; species occurring in SAVANNAH are capitalized; species occurring in riparian habitats are underlined; line thickness and line background color refer to parsimony reconstructions; pie charts (only shown for nodes relevant for discussion) refer to Bayesian reconstructions.

Figure 5

Migratory behavior mapped onto the Elaenia tree topology derived from concatenated dataset with species-level lineages reduced to one representative;austral migrant species are underlined with a solid line, partially migratory species are underlined with a broken line; sedentary species are not underlined; line thickness refers to parsimony reconstructions; pie charts (only shown for nodes relevant for discussion) refer to Bayesian reconstructions.

Figure 6

Age estimates of Elaenia speciation events mapped onto the concatenated tree topology using a 2%/million years (MY) molecular clock rate; scale in MY; error bars at nodes refer to divergence range between taxa; neighboring nodes were merged in cases where both upper and lower divergence bound of one node falls inside the range of the neighbour; scale at bottom indicates millions of years before present.