Evolutionary innovation and diversification of carotenoid‐based pigmentation in finches

Abstract

The ornaments used by animals to mediate social interactions are diverse, and by reconstructing their evolutionary pathways we can gain new insights into the mechanisms underlying ornamental innovation and variability. Here, we examine variation in plumage carotenoids among the true finches (Aves: Fringillidae) using biochemical and comparative phylogenetic analyses to reconstruct the evolutionary history of carotenoid states and evaluate competing models of carotenoid evolution. Our comparative analyses reveal that the most likely ancestor of finches used dietary carotenoids as yellow plumage colorants, and that the ability to metabolically modify dietary carotenoids into more complex pigments arose secondarily once finches began to use modified carotenoids to create red plumage. Following the evolutionary "innovation" that enabled modified red carotenoid pigments to be deposited as plumage colorants, many finch species subsequently modified carotenoid biochemical pathways to create yellow plumage. However, no reversions to dietary carotenoids were observed. The finding that ornaments and their underlying mechanisms may be operating under different selection regimes-where ornamental trait colors undergo frequent reversions (e.g., between red and yellow plumage) while carotenoid metabolization mechanisms are more conserved-supports a growing empirical framework suggesting different evolutionary patterns for ornaments and the mechanistic innovations that facilitate their diversification.

Expression of a carotenoid‐modifying gene and evolution of red coloration in weaverbirds (Ploceidae)

“…Despite this, intensely red‐coloured integument (plumage, beak, skin) has a surprisingly limited and patchy distribution across birds (Aves). Even in clades where red carotenoid coloration is common, for example widowbirds and bishops (Prager & Andersson, ), New World blackbirds (Friedman, McGraw, & Omland, ) and cardueline finches (Ligon, Simpson, Mason, Hill, & McGraw, ), its absence in several lineages is not associated with any obvious and relevant ecological or behavioural differences from their red‐coloured relatives. This suggests that some genetic or physiologically “hard‐wired” constraint is at play and that C4‐ketolation of integumentary carotenoids is likely to be a major hurdle for the evolution of red pigmentation.…”

Synergistic selection regimens drive the evolution of display complexity in birds of paradise

“…In passerines like birds of paradise, these colours are exclusively generated by diet‐derived carotenoid pigments (Goodwin, ). This means that generating red and yellow ornaments relies not only on an individual's ability to acquire food, but also on converting dietary forms into usable pigments along numerous metabolic pathways (Cardoso & Mota, ; Ligon et al., ). As a result, carotenoid colours sometimes function as condition‐dependent badges used to negotiate male–male competition (Peek, ; Pryke & Andersson, ).…”

“…This F I G U R E 3 Signal space schematic depicting how female choice (red arrow), direct male-male competition (blue arrow) and display habitat (orange arrow) each influence visual displays in birds of paradise. The four plotted points correspond to four representative species that exemplify these effects: (1) Manucodia chalybatus, a non-lekking species that displays alone in the canopy, is sexually monochromatic and performs a relatively simple display, (2) male Astrapia rothschildi, which display in the canopy at a solitary lek, are highly sexually dichromatic, (3) Paradisaea rubra gather in large numbers to display in canopy leks and employ numerous carotenoid ornaments, and (4) Parotia carolae have the most complex dance routines of all, performing in groups of up to 6 on their forest floor leks [Colour figure can be viewed at wileyonlinelibrary.com] means that generating red and yellow ornaments relies not only on an individual's ability to acquire food, but also on converting dietary forms into usable pigments along numerous metabolic pathways (Cardoso & Mota, 2008;Ligon et al, 2016). As a result, carotenoid colours sometimes function as condition-dependent badges used to negotiate male-male competition (Peek, 1972;Pryke & Andersson, 2003).…”

“…For example, sexual selection for colourful males encompasses a diverse range of evolutionary processes that generate dichromatism in different ways. Among the many possibilities are exaggerating the degree to which different melanins are deposited across the body (Bókony, Liker, Székely, & Kis, 2003;Galván, 2008), and/or increasing colour complexity by evolving novel metabolic pathways to process diet-derived carotenoids into new hues (Badyaev, Hill, & Weckworth, 2002;Goodwin, 1980;Ligon, Simpson, Mason, Hill, & McGraw, 2016). Because these different pigment origins for colour represent developmentally distinct pathways, they have the potential to act as individual components of the modular visual display (Hebets et al, 2016).…”

Microstructures amplify carotenoid plumage signals in colorful tanagers

“…However, in Ramphocelus it appears that R. f. icternonotus and R. flammigerus evolved to use dietary carotenoids (yellow & orange) from a likely ancestral state of metabolized (red) carotenoids ( Figure 3, Figure S1; this is the most parsimonious explanation, particularly given that the Ramphocelus clade has red-colored sister species (Burns and Racicot 2009)). In fringillid finches, a model system for plumage evolution, there are no documented reversions from metabolized to dietary pigments (Ligon et al 2016). New world blackbirds (Icteridae) convergently evolved red plumage from yellow six times but never in the reverse direction (Friedman et al 2011).…”