Molecular phylogenetics of Doraditos (Aves, Pseudocolopteryx): Evolution of cryptic species, vocal and mechanical sounds

Abstract

While bird vocalizations (produced by the syrinx) have been the focus of countless studies, mechanical sounds (produced by external body structures) have received much less attention. In particular, the evolutionary interplay between these two modes of acoustic communication remains largely unstudied. Here, we present the first species‐level molecular phylogeny of the doraditos (Pseudocolopteryx), reconstruct the evolutionary history of acoustic vocal and non‐vocal characters, elucidate their relationship to feather modifications and aerial displays, and explore the influence of acoustics in the speciation of cryptic species. Our well‐resolved phylogeny using four genes (ND2, COI, MB and ODC), recovered the monophyly of Pseudocolopteryx, resolving the relationships among its five species: ((((P. sclateri) P. acutipennis) P. dinelliana) P. citreola, P. flaviventris). Repetition and translocation of acoustic elements were commonplace in the evolution of Pseudocolopteryx. Songs were composed of introductory syllables and a final flourish. Bill‐snapping sounds of P. sclateri were functionally homologous to introductory vocal syllables of the other species. The song of P. dinelliana evolved to high levels of complexity and repetition and is the syntactically most complex song in Pseudocolopteryx (and perhaps in the Tyrannidae). Aerial displays, mechanical wing sounds and modifications of primary feathers coevolved in three species: P. sclateri, P. acutipennis and P. dinelliana. Wing sounds documented for P. acutipennis and P. dinelliana differed markedly, and their production mechanisms might differ. The two cryptic and sibling species P. flaviventris and P. citreola diverged ∽60,000 Ya were not reciprocally monophyletic and are a case of extremely rapid evolutionary acoustic differentiation with morphological stasis.

Biogeography, speciation and niche evolution of doraditos (Aves: Pseudocolopteryx)

“…However, the Hennigian perspective has been criticized for its unrealistic and biased view of the complexities in the evolutionary transformations of organisms, and especially for denying the real existence of ancestors (Cavalier-Smith, 2010;Mayr, 1973). The divergence between P. citreola and P. flaviventris has been dated at about 60,000 years ago (Jordan et al, 2021). This extreme recentness might be overestimated as RADseq data indicate an older divergence time between these cryptic species (Jordan et al in prep.).…”

“…The cryptic species P. citreola and P. flaviventris show minimal genetic divergence (Jordan et al, 2021;Jordan et al in prep. ) and strong vocal differences (Abalos & Areta, 2009;Jordan et al, 2021). In a scenario of peripatric speciation, a small peripheral population of the more broadly distributed P. citreola would have become geographically isolated from the main population, subsequently diverging and giving rise to P. flaviventris.…”

“…The five species of doraditos (Crested Doradito Pseudocolopteryx sclateri, Subtropical Doradito P. acutipennis, Dinelli's Doradito P. dinelliana, Warbling Doradito P. flaviventris and Ticking Doradito P. citreola) are Neotropical flycatchers of open areas associated to different extents to aquatic habitats. They are wholly South American, but their richness peaks in the southern cone, where all species can be found (Fitzpatrick, 2004;Jordan et al, 2021;Ridgely & Tudor, 1989). The scattered information on the breeding distribution of doraditos seems to show a low degree of geographic overlap between species (Claessens & de Guyane, 2015;Herzog et al, 2016;Jaramillo, 2003;Pearman & Areta, 2020), while the literature regarding the seasonal movements is sparse and inconclusive, and the wintering grounds remain scarcely known for all the species (Fitzpatrick, 2004;Ridgely & Tudor, 1989) (see Section 2.1 below for details).…”

“…The species‐level phylogenetic relationships of Pseudocolopteryx have recently been clarified (Jordan et al., 2021). The sibling species P. citreola and P. flaviventris are sister to P. dinelliana , and this clade is sister to P. acutipennis .…”

“…(b) Increasing environmental overlap with increasing phylogenetic distance is interpreted as rapid niche evolution and the rejection of niche conservatism as a tendency. Phylogenetic data fromJordan et al (2021). See FigureS4for comparisons controlling for post-speciational (human-induced) changes in P. acutipennis.4.1 | Distribution and migration of doraditosThe two species exhibiting longer phylogenetic branches, P. sclateri and P. acutipennis, are widespread breeders and do not appear to be associated to any particular biogeographic region.…”