A comprehensive multilocus phylogeny of the Neotropical cotingas (Cotingidae, Aves) with a comparative evolutionary analysis of breeding system and plumage dimorphism and a revised phylogenetic classification
Graphical abstract
Introduction
The cotingas (Cotingidae) are a diverse radiation of Neotropical, suboscine frugivores and omnivores that includes 66 species in 25 genera (Snow, 1982, 2004; Kirwan and Green, 2012). Cotingas are well known for their diversity in sexual dimorphism, plumage coloration and ornamentations, vocalizations, display behaviors, and breeding systems. The family includes species with concentrated leks (e.g. Guianan Cock-of-the-Rock, Rupicola rupicola), dispersed leks (e.g. Phoenicircus red cotingas), solitary leks (e.g. Procnias bellbirds), socially monogamous species (e.g. Ampelion cotingas, Phytotoma plantcutters, and Pipreola fruiteaters, etc.), and even group living territorial species with helpers at the nest (Purple throated Fruitcrow, Querula purpurata).
Cotingas also encompass a great diversity of avian plumage coloration mechanisms. Various cotingas produce plumage colors with (1) eumelanin and phaeomelanin pigments, (2) a tremendous diversity of dietary and physiologically modified carotenoid pigments, (3) spongy, medullary structural coloration in barb rami, (4) iridescent barbule structural coloration (in Cephalopterus umbrellabirds), and (5) combinations of barb structural coloration and carotenoid pigments (e.g. green plumages in Pipreola and female Procnias) (Prum et al., 1998, Prum et al., 1999, Prum et al., 2012, Saranathan et al., 2012).
Variation in cotinga plumage is not restricted to the coloration alone. Many male cotingas have unusual plumage ornaments like the vertical crests of Cocks-of-the-Rock, or the forward-bending crown feathers that give the Cephalopterus umbrellabirds their common name. Cotingas also exhibit a wide diversity of fleshy skin ornaments which includes the structurally colored bare blue crowns of Perisocephalus tricolor, the blue face and neck skin of Gymnoderus foetidus, the bare green throat skin of Procnias nudicollis (Prum and Torres, 2003), the bare black throat patch with dozens of thin, wormy wattles of Procnias averano, the single, feathered nasal wattle of Procnias alba (Burton, 1976), the three, bare black nasal and rictal wattles of Procnias tricarunculata, and the elongate bare or feathered breast wattle of the umbrellabirds.
Cotingas also vary strikingly in their vocal behavior and acoustic signaling. A few species vocalize very infrequently (Carpodectes nitidus, C. antoniae, and Xipholena sp.) (Kirwan and Green, 2012). However, the Procnias bellbirds and Lipaugus pihas produce some of the loudest bird vocalizations in the world (Nemeth, 2004). Procnias bellbirds are also the only members of the suboscine clade demonstrated to exhibit vocal learning (Saranathan et al., 2007, Kroodsma et al., 2013). In order to produce these diverse and variable vocal signals, the cotingas are tremendously diverse in syringeal morphology, and many genera are identifiable by unique syringeal morphology (Prum, 1990, Prum, unpubl. data). Several cotinga species also produce conspicuous mechanical wing-sounds as part of their courtship displays (e.g. Rupicola, Phoenicircus, and Cotinga) (Snow, 2004).
Further, cotingas vary in the relation between breeding system and sexual plumage dimorphism. Cotingas include polygynous, sexually monomorphic species that advertise with largely acoustic signals (eg. Lipaugus), monogamous, monomorphic species (eg. Ampelion, Zaratornis), monogamous, dimorphic species (eg. Pipreola, Phytotoma), and polygynous, dimorphic species (e.g. Procnias, Cotinga). Ohlson et al. (2007) first tested the hypothesis that the sexually dimorphic, polgynous state in the cotingas was derived from a sexually monomorphic, monogamous root state (Snow, 1973) but limited taxon sampling and poor resolution at the base of their tree resulted in equivocal reconstructions.
Comparative analysis of the evolution of the morphological, behavioral, and ecological diversity of cotingas requires a comprehensive species-level phylogeny of the family. Anatomical and molecular phylogenetic studies have largely resolved the previously confusing limits of the cotinga clade (Prum, 1990, Prum et al., 2000, Johansson et al., 2002, Ohlson et al., 2007, Ohlson et al., 2013, Tello et al., 2009), but previous phylogenetic analyses have not attempted to reconstruct the relationships among a comprehensive sample of cotinga species. Previous studies have also focused on analyzing single locus or concatenated data sets that assume gene-tree concordance.
Here, we present a comprehensive phylogeny of the cotingas based on molecular data for up to ~7500 base pairs of nuclear introns (MYO, G3PDH), exons (RAG-1, RAG-2), and mitochondrial genes (CYT-B, ND2) for a sample of 61 species in all 25 cotinga genera, and 22 species of suboscine outgroups. Our cotinga sample includes all but four currently recognized species in the family: Handsome Fruiteater Pipreola formosa and Golden-breasted fruiteater Pipreola aureopectus, Chestnut-capped Piha Lipaugus weberi, and Grey-winged Cotinga Tijuca condita (all are narrow endemics with few specimens available). We analyze these phylogenetic data using a Bayesian species tree method, and concatenated Bayesian and maximum likelihood methods. We then present a comparative phylogenetic analysis of the evolution of cotinga breeding systems and sexual plumage dimorphism. Specifically, we test the hypothesis that increased levels of sexual selection associated with polygyny have fostered the evolution of sexual dimorphism in plumage coloration.
Traditionally, the cotinga family has included an even wider diversity of species than are currently placed in Cotingidae (Ridgway, 1907, Hellmayr, 1929, Snow, 1973, Snow, 1979). The historically broader limits to the family included becards (Pachyrampus), tityras (Tityra), purpletufts (Iodopleura), various genera of mourners (Laniisoma, Laniocera, Rhytipterna, and Casiornis), and often the Sharpbill (Oxyruncus cristatus). The traditional cotingas excluded the plantcutters (Phytotoma), which were often placed in the Phytotomidae (Snow, 1973, Snow, 1982, Lanyon and Lanyon, 1988), and Rupicola which was placed in Rupicolidae (Hellmayr, 1929).
On the basis of syringeal anatomy, Ames (1971) removed Pachyrampus, Tityra, Rhytipterna, and Casiornis from the cotingas, and transferred them to the tyrant flycatchers (Tyrannidae). Using cladistic analysis of syringeal characters and protein electrophoresis, Lanyon and Lanyon (1988) moved Phytotoma into the Cotingidae near the Andean Ampelion species, as first suggested by Küchler (1936). In the first phylogenetic test of the monophyly of cotingas, Prum (1990) identified a clade of cotingas based on a derived insertion of an extrinsic syringeal muscle – M. tracheolateralis – on the lateral syringeal membrane between the A1 and B1 supporting elements. However, unrecognized evolutionary derivation (Lipaugus) and loss (Tityra) of complex intrinsic syringeal muscles contributed ambiguity to diagnosis of cotinga monophyly. Prum et al. (2000) largely confirmed the monophyly of the cotinga clade with an analysis of sequences of the mitochondrial gene cytochrome-B (CYT-B). However, they erroneously placed Oxyruncus within the cotinga clade based on an untranscribed nuclear copy of CYT-B (Johansson et al., 2002). Prum et al. (2000) confirmed Ames’ hypothesis that Tityra is closely related to Pachyramphus within the Schiffornis group– a novel clade made of former members of the cotinga, manakin, and flycatcher families (Prum and Lanyon, 1989).
Ohlson et al. (2007) provided a well-resolved phylogeny of 26 cotinga species in 22 genera based on ∼2100 base pairs of nuclear and mitochondrial DNA (Fig. 1). They identified four main clades: (1) a montane fruiteater clade including Pipreola and Ampelioides as the sister group to the rest of the family, (2) the Ampelion clade including Ampelion, Doliornis, Zaratornis, and the Phytotoma plantcutters as the next sister group to the remainder of the family, (3) the Rupicola–Phoenicircus clade, and (4) a diverse clade of the ‘core’ cotingas including the fruitcrows, two clades of pihas, and a clade of ‘canopy’ cotingas. Tello et al. (2009) analyzed ∼4000 bases of the nuclear RAG-1 and RAG-2 genes for a slightly different sample of 25 cotinga species in 23 cotinga genera. The Tello et al. (2009) phylogeny identified many of the same broad clades as Ohlson et al. (2007) but with a few slight differences: Snowornis was placed as the sister group to the Rupicola–Phoenicircus clade; this clade was sister group to the Ampelion clade; and the genus Carpornis was placed as the sister group to this larger clade. Within the fruiteaters, the Ampelion clade, and the fruitcrows, the phylogenetic relationships of Tello et al. (2009) and Ohlson et al. (2007) are highly congruent, but relationships between Lipaugus, Cotinga, and Procnias were inconsistent between the two studies (Fig. 1).
Most recently, Ohlson et al. (2013) analyzed three introns and two exons (∼6300 bp) across 14 cotinga species (14 genera), and supported different phylogenetic relationships from both Tello et al. (2009) and Ohlson et al. (2007); the Ampelioides–Pipreola fruiteater clade was reconstructed as sister to all other cotingas in all three, but they inferred different relationships among the Snowornis–Rupicola clade, the ‘core’ cotinga clade, and the Ampelion clade. Further, Ohlson et al. (2013) placed Lipaugus within the ‘core’ cotingas, while Tello et al. (2009) placed it as the sister group to the rest of the clade. Regardless, inadequate taxon sampling in all prior analyses has limited overall resolution (Fig. 1).
A few recent taxonomic changes have been recommended. Based on substantial genetic differentiation (Prum et al., 2000) and differences in syringeal morphology, Prum (2001) proposed the genus Snowornis for two Andean piha species-cryptolophus and subalaris – that were formerly in the genus Lipaugus. Ohlson et al. (2007) confirmed that Snowornis is monophyletic, and not closely related to Lipaugus. In sum, previous phylogenetic studies of cotingas have not included enough taxa to test the monophyly of cotinga genera. This is partly because cotinga genera are so highly split – an average of only 2.6 species per genus – as a consequence of taxonomic splits that reflect extreme diversity in secondary sexual traits.
Section snippets
Taxon and character sampling
We sampled frozen or preserved tissue samples of 63 specimens of 49 different cotinga species (Table 1). Although we had no tissue for the species, sequences for two nuclear and one mitochondrial genes from this species were available for Tijuca atra through GenBank (Ohlson et al., 2007). An additional 12 species were represented by 21 toepad samples from museum study skins (collected 1926–1970). In order to assess geographic variation within some cotinga species, multiple populations were
Data partitioning
For our species tree analysis, partitioning schemes were evaluated for each locus separately; PartitionFinder indicated that the maximally partitioned scheme S3 (with each codon position on different partitions) was significantly preferred for all protein-coding loci with the exception of RAG2 (ND2, ΔBICS2–S3 = 133; CYTB, ΔBICS2–S3 = 94; RAG1, ΔBICS2–S3 = 22). For RAG2, the intermediately partitioned scheme S2 (with the first two codon positions grouped together and the third separately) was
Discussion
This comprehensive study of the relationships among the Neotropical cotingas establishes a strongly supported phylogenetic hypothesis for this highly diverse radiation. Our findings establish the first phylogenetic hypotheses for intrageneric relationships within the Cotinga, Lipaugus, Pipreola, and Procnias clades, and the first phylogenetic placement of the highly distinctive Swallow-tailed Cotinga Phibalura flavirostris.
Acknowledgments
We thank the numerous researchers whose field collection efforts made this research possible including: George F. Barrowclough, Steve Cardiff, Terry Chesser, Mario Cohn-Haft, Tristan Davis, Andrew Kratter, Patricia Escalante Pliego, Cecilia Fox, John O’Neill, Ted Parker, Richard Prum, Nate Rice, Mark Robbins, Gary Rosenberg, Peter E. Scott, Doug Stotz, Tom Schulenberg, David Willard, and others.
Tissue loans were kindly received from the American Museum of Natural History, New York (AMNH), the
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Current address: Department of Ecology and Evolutionary Biology, Fuller Evolutionary Biology Program, Cornell University, and Cornell Laboratory of Ornithology, 159 Sapsucker Woods Road, Ithaca, NY 14850, USA.