Rapid phenotypic evolution during incipient speciation in a continental avian radiation

Abstract

Adaptive radiations have helped shape how we view animal speciation, particularly classic examples such as Darwin's finches, Hawaiian fruitflies and African Great Lakes cichlids. These 'island' radiations are comparatively recent, making them particularly interesting because the mechanisms that caused diversification are still in motion. Here, we identify a new case of a recent bird radiation within a continentally distributed species group; the capuchino seedeaters comprise 11 Sporophila species originally described on the basis of differences in plumage colour and pattern in adult males. We use molecular data together with analyses of male plumage and vocalizations to understand species limits of the group. We find marked phenotypic variation despite lack of mitochondrial DNA monophyly and few differences in other putatively neutral nuclear markers. This finding is consistent with the group having undergone a recent radiation beginning in the Pleistocene, leaving genetic signatures of incomplete lineage sorting, introgressive hybridization and demographic expansions. We argue that this apparent uncoupling between neutral DNA homogeneity and phenotypic diversity is expected for a recent group within the framework of coalescent theory. Finally, we discuss how the ecology of open habitats in South America during the Pleistocene could have helped promote this unique and ongoing radiation.

The multiple applications of DNA barcodes in avian evolutionary studies

“…One of the most striking cases of low interspecific divergence and lack of reciprocal monophyly in DNA barcodes among Neotropical birds is that of the southern capuchino seedeaters, a clade of eight species of Sporophila that are mostly sympatric (Kerr et al 2009a;Campagna et al 2010). This group shows remarkably high plumage colour divergence among males, which also produce distinctive vocalizations, suggesting that species-level designations to them are correct (Campagna et al 2012a). There is also evidence that males from these species react more strongly to male conspecific vocalizations than to hetero-specific ones, indicating that the interspecific differences in vocalizations are in fact detected by the birds, supporting the notion that these are different species (Benites et al 2015).…”

“…A more extensive analysis that included more mitochondrial markers, microsatellites, and nuclear gene sequences showed that this group of species constitutes a recent radiation with incomplete lineage sorting and hybridization still occurring among these species despite the large morphological and behavioural differentiation (Campagna et al 2012a(Campagna et al , 2013. More recently, Campagna et al (2015) used a reduced-representation genomic approach to examine a much larger number of loci and still could not find genetic markers significantly differentiated among species of southern capuchinos.…”

“…Low or null genetic divergence in COI with noticeable phenotypic differentiation between different species has been linked to events of recent radiations (Liebers et al 2004;Campagna et al 2010Campagna et al , 2012aCampagna et al , 2015. In turn, some cases of deep genetic divergence in DNA barcodes within species were further investigated with other molecular and phenotypic markers and were found to be cases of evolutionarily isolated lineages, some of which even deserved species status (Sanin et al 2009;Efe et al 2009;Kerr and Dove 2013;Lavinia et al 2015a;García et al 2016).…”

Continental phylogeography of an ecologically and morphologically diverse Neotropical songbird, Zonotrichia capensis

“…ND2, 16 S and MELK were amplified following PCR conditions outlined for CR, with the annealing temperatures and MgCl 2 concentrations specified in the Additional file 1. COI amplification was conducted following Kerr et al [37], while PCRs for CHD1Z and Fib5 followed Campagna et al [38]. The small CR fragments amplified from toe pad DNA were electrophoresed in 0.5% agarose gels, and then excised and purified by the “freeze-squeeze” method [39].…”

Loss of sexual dimorphism is associated with loss of lekking behavior in the green manakinXenopipo holochora

“…Between the two sub-species isolated by the Andes mountains, there was well-defined divergence in plumage coloration, which may be indicative of incipient speciation (Campagna et al 2012). Within each subspecies, however, sexual dichromatism was virtually nonexistent.…”