Paulo G. Mota

Birdsong, sexual selection, and the flawed taxonomy of canaries, goldfinches and allies

Sexual signals are often diagnostic of closely related species, and their taxonomic value at higher phylogenetic levels is often discussed. Complex signals such as birdsong are potentially rich in information regarding evolutionary history. However, natural or sexual selection, if pervasive enough, might distort that information. This has seldom been evaluated. We tested how ecological effects impact on the phylogenetic information of birdsong using a real case of flawed taxonomy: the reciprocal polyphyly of the genera Serinus and Carduelis. Major axes (principal components) of between-species song variation were not related to body size or habitat type. The main axis of song variation, reflecting syllable complexity and song length, was related to ecological indexes of sexual selection (latitude and ecological breadth), resulting in a positive latitudinal gradient in song elaboration. Song significantly supported monophyly over polyphyly for these genera, despite some song data having high phylogenetic signal (relative to the correct, polyphyletic phylogeny). Thus, the presence of high phylogenetic signal did not guarantee reliable taxonomic information at the genus level. The misleading phylogenetic information appears related to the latitudinal gradient in song elaboration plus the traditional Serinus and Carduelis spp. differing in latitude. We conclude that selection, in this case sexual selection, can pervasively distort the phylogenetic information even of complex and potentially information-rich signals.

Intense extrapair behaviour in a semicolonial passerine does not result in extrapair fertilizations

Sperm competition is a strong force on the evolution of mating behaviour of animals, particularly birds. In monogamous birds extrapair behaviour is one main source of variation in the reproductive success of males, which has caused the evolution of paternity guards as well as strategies by females to increase the genetic quality of their descendants. We investigated the importance of sperm competition in the reproductive behaviour of serins, Serinus serinus. Male serins guarded their mates and also copulated frequently, indicating that sperm competition has been an important selective force affecting their mating behaviour. Females were frequently approached and chased by extrapair males that attempted extrapair copulations. However, females refused almost every attempt by extrapair males. No extrapair paternity was detected in the population, in spite of the intense extrapair behaviour of males. This supports the view that females keep strong control over paternity, and that in this population they do not seem to obtain genetic benefits from extrapair copulations. We discuss why the presence of high levels of sexual competition may not be reflected in extrapair paternity.

Ultraviolet reflectance influences female preference for colourful males in the European serin

Avian plumage colouration is one of the most impressive displays in nature and is frequently used as sexual signal. There is now considerable evidence that females consistently prefer males with the most elaborated colour displays. Bird colour vision expands into the ultraviolet (UV) range, which prompted several studies to test the importance of UV in mate choice, revealing that females are affected by the UV light component. These studies were mostly performed on structural plumage, whereas carotenoid-based plumage was rarely considered, although it also has a typical reflection peak in the UV. Our study tested the female choice over male yellow colouration, and whether it is influenced by UV removal, in the European serin (Serinus serinus), a sexually dichromatic cardueline finch, with males showing a conspicuous carotenoid-based yellow plumage. We shows that females preferred yellower males and that male attractiveness was lost when the UV colouration was blocked, with either of the UV-blocking techniques used. The results of our study indicate that the UV component of carotenoid colouration is important in the female mate assessment in serins and highlights the importance of considering colour perception in avian mate choice.

High-density lipoprotein receptor SCARB1 is required for carotenoid coloration in birds

Significance The yellow, orange, and red colors of birds are produced through the deposition of carotenoid pigments into feathers and skin, and often function as signals in aggressive interactions and mate choice. These colors are hypothesized to communicate information about individual quality because their expression is linked to vital cellular processes through the mechanisms of carotenoid metabolism. To elucidate these mechanisms, we carried out genomic and biochemical analyses of the white recessive canary breed, which carries a heritable defect in carotenoid uptake. We identified a mutation in the SCARB1 gene in this breed that disrupts carotenoid transport function. Our study implicates SCARB1 as a key mediator of carotenoid-based coloration and suggests a link between carotenoid coloration and lipid metabolism. Yellow, orange, and red coloration is a fundamental aspect of avian diversity and serves as an important signal in mate choice and aggressive interactions. This coloration is often produced through the deposition of diet-derived carotenoid pigments, yet the mechanisms of carotenoid uptake and transport are not well-understood. The white recessive breed of the common canary (Serinus canaria), which carries an autosomal recessive mutation that renders its plumage pure white, provides a unique opportunity to investigate mechanisms of carotenoid coloration. We carried out detailed genomic and biochemical analyses comparing the white recessive with yellow and red breeds of canaries. Biochemical analysis revealed that carotenoids are absent or at very low concentrations in feathers and several tissues of white recessive canaries, consistent with a genetic defect in carotenoid uptake. Using a combination of genetic mapping approaches, we show that the white recessive allele is due to a splice donor site mutation in the scavenger receptor B1 (SCARB1; also known as SR-B1) gene. This mutation results in abnormal splicing, with the most abundant transcript lacking exon 4. Through functional assays, we further demonstrate that wild-type SCARB1 promotes cellular uptake of carotenoids but that this function is lost in the predominant mutant isoform in white recessive canaries. Our results indicate that SCARB1 is an essential mediator of the expression of carotenoid-based coloration in birds, and suggest a potential link between visual displays and lipid metabolism.

What is the value of a yellow patch? Assessing the signalling role of yellow colouration in the European serin

Sexual selection promotes the evolution of signals, many of which can reliably indicate condition, health or good genes of individuals. In order to be evolutionarily stable, indicator signals must be costly to produce. Carotenoid colouration evolved in many species by sexual selection. Carotenoids besides acting as pigments have been implicated in immune defence and antioxidation which makes them likely candidates for honest signalling. A trade-off for carotenoid availability was proposed as the basis for signal honesty. Alternatively, it was suggested that carotenoid colouration is not advertising the presence of the pigment per se, but the quality of antioxidant resources which then affect carotenoid concentration. One possibility is that carotenoid-based colouration could signal colourless antioxidant mechanisms, which are partially regulated by vitamins. β-Carotene is one of the most common precursors of vitamin A and, although present in bird diet, is not available for feather colouration. If an indirect association exists between carotenoid signal and condition, then manipulation of β-carotene concentration could reveal that this link is indirect. We tested this by conditioning the availability of β-carotene in the diet of a cardueline finch with yellow carotenoid colouration during moult. β-Carotene-supplemented males had higher plasma carotenoid concentration and higher response to a cellular immunity challenge (phytohaemagglutinin (PHA)) than control males. β-Carotene-supplemented males also had more saturated plumage colouration and were preferred by females in a mate choice test. Our results support the possibility of an indirect role for yellow carotenoid colouration.

Similar preferences for ornamentation in opposite- and same-sex choice experiments.

Selection due to social interactions comprises competition over matings (sexual selection stricto sensu) plus other forms of social competition and cooperation. Sexual selection explains sex differences in ornamentation and in various other phenotypes, but does not easily explain cases where those phenotypes are similar in males and females. Understanding such similarities requires knowing how phenotypes influence nonsexual social interactions as well, which can be very important in gregarious animals, but whose role for phenotypic evolution has been overlooked. For example, ‘mate choice’ experiments often found preferences for ornamentation, but have not assessed whether those are strictly sexual or are general social preferences. Using choice experiments with a gregarious and mutually ornamented finch, the common waxbill (Estrilda astrild), we show that preferences for ornamentation in the opposite‐sex also extend to same‐sex interactions. Waxbills discriminated between opposite‐ and same‐sex individuals, but most preferences for colour traits were similar when interacting with either sex. Similar preferences in sexual and nonsexual associations may be widespread in nature, either as social adaptations or as by‐product of mate preferences. In either case, such preferences may set the stage for the evolution of mutual ornamentation and of various other similarities between the sexes.

Darwin's sexual selection theory - a forgotten idea

Resumo A teoria de seleccao sexual de Darwin e muito menos conhecida que a teoria de seleccao natural e permaneceu praticamente desconhecida durante cerca de um seculo. Sendo hoje uma das teorias cientificas mais prolificas na biologia, e muito interessante, cientifica e epistemologicamente, entender porque permaneceu ignorada durante tanto tempo. Proponho que uma parte do seu abandono inicial teve, em parte, a ver com preconceitos sociais da epoca. Mas, porventura a razao mais significativa teve a ver com a dificuldade do conceito. Foi necessario um importante desenvolvimento teorico com a introducao de um pensamento populacional, que ja estava presente em Darwin, e uma perspectiva de evolucao centrada no gene, a par de desenvolvimentos formais, como a teoria de jogos, para se tornar possivel desenvolverem e testar hipoteses que confirmassem a teoria. Nesta perspectiva, a visao de Darwin adquire uma dimensao ainda mais extraordinaria. Palavras-chave Darwin; seleccao sexual; teoria cientifica; teoria de jogos; evolucao.

Competitive advantages of the red-billed leiothrix (Leiothrix lutea) invading a passerine community in Europe

The establishment of an introduced species is an important step of the invasion pathway. Often species become established because of their superior competitiveness over the native community or by occupying empty niches. Recently, the red-billed leiothrix Leiothrix lutea has become established in some European natural-woods, which can be quite relevant for nature conservation considering its position among the seven exotic bird species with highest negative impact in bird communities. We assessed which European-native species are more likely to compete with the leiothrix (i.e. potential competitors) based on their structural size and diet composition. Also, we evaluated the competitive advantages of the leiothrix, relatively to its potential competitors, that may allow its successful establishment, considering two approaches: exploratory behaviour and foraging morphology. Two species showed great similarity in structural size with the leiothrix, and also presented great similarity in diet composition, which makes them potential competitors: the robin Erithacus rubecula and the blackcap Sylvia atricapilla. The exploratory behaviour of the leiothrix did not differ from those of its potential competitors. However, the leiothrix presented more efficient foraging morphology than their potential competitors. Our results support the hypothesis of an establishment process by competitive advantage over native species rather than an opportunistic occupation of an empty ecological niche. The establishment of the leiothrix in European natural-habitats, and not in highly disturbed habitats as other invasive species, may constitute a new challenge for conservation.

A test of the effect of testosterone on a sexually selected carotenoid trait in a cardueline finch

A great number of secondary sexual traits are assumed to have evolved as honest signals of individual quality. It is known that androgens regulate many male secondary traits as well as reproductive behavior. The expression of melanin-based coloration is modulated by androgens, particularly testosterone, and there is some evidence that carotenoid-based coloration may also be under androgen control. In the European serin, Serinus serinus, male carotenoid-based plumage coloration is a sexually selected trait, subjected to female choice. In this experiment, we investigated if testosterone influences the expression of this trait by manipulating testosterone levels during molt and assessing how it affected plumage color expression after molt. We found that testosterone had only a negative effect on the size of the yellow ornament. Our experiment shows that testosterone had a limited effect on carotenoid-based coloration of a cardueline finch.

Evidence for multiple functions in a sexually selected ornament

In gregarious animals, social interactions frequently take the form of dominance hierarchies that maintain stable relationships between individuals, and settle disputes without extra costs. Traits that function as signals of status can play an important role in mediating interactions among individuals, both in social and in sexual contexts. Carotenoid ornaments are more generally assumed to be sexually selected and not so relevant to general social contexts. However, it is possible for them to function in social contexts if they signal socially relevant aspects. Here we experimentally analysed social dominance and resource control in male groups of a gregarious species, the European serin, Serinus serinus, in relation to a sexual ornament. We tested whether yellow carotenoid-based plumage coloration, age, body size and testosterone were predictors of social dominance over a nonsexual resource (i.e. feeding context). We showed that dominance hierarchies were steep and were related to testosterone levels and ornamental coloration, particularly the male yellow carotenoid-based crown patch. Our results suggest that carotenoid-based colour and testosterone levels can be reliable predictors of social status in agonistic encounters in groups of male serins. Moreover, together with previous work on the sexual function of male coloration, this study provides evidence that male serin yellow coloration has a dual function in both sexual and nonsexual contexts. These results raise the possibility that this ornament may have evolved and be maintained via social selection over social competition/cooperation for reproductive opportunities and ecological resources.