Gonçalo C. Cardoso

Birdsong Performance and the Evolution of Simple (Rather than Elaborate) Sexual Signals

Sexual signals are often elaborate as a result of sexual selection for signals of individual quality. Contrary to expectation, however, the elaboration of signals such as birdsong is not related to the strength of sexual selection across species. With a comparative study across wood warblers (family Parulidae), we show a compromise between advertising the performance of trills (syllable repetitions) and song complexity, which can result in the evolution of simple, rather than elaborate, song. Species with higher trill performance evolved simple songs with more extensive trilled syntax. This advertises trill performance but reduces syllable diversity in songs. These two traits are commonly sexually selected in songbirds, but indexes of sexual selection were not related to either in wood warblers. This is consistent with sexual selection targeting different traits in different species, sometimes resulting in simple signals. We conclude that the evolution of sexual signals can be unpredictable when their physiology affords multiple or, as here, opposing ways of advertising individual quality.

On the relation between loudness and the increased song frequency of urban birds

Songbirds often sing at higher frequency (pitch) in urban, noise-polluted areas, which reduces acoustic masking by low-frequency anthropogenic noise. Such frequency shifts, however, are less efficient at overcoming background noise than simply singing louder. Therefore, it was suggested that high-frequency singing might not be a functional adjustment to noise, but a physiological consequence of singing louder (also known as the Lombard effect). We tested for the first time the main tenet of this hypothesis, for birdsong whether increasing sound amplitude has a concomitant effect on song frequency, using a representative species with higher urban minimum frequency, the dark-eyed junco, Junco hyemalis. The frequency bandwidth of songs and syllables increased with amplitude, involving lower minimum frequency in louder songs and syllables. Therefore, louder singing does not explain the higher minimum frequency of urban dark-eyed juncos. Amplitude and peak frequency were weakly positively related across but not within songs, suggesting that increased frequency is not an obligatory outcome of singing louder. Instead, birds may adjust both amplitude and frequency in response to changing noise or motivation across songs. Our results suggest that adjustments in song frequency and amplitude are largely independent and, thus, can be complementary rather than alternative vocal adjustments to noise. We discuss oscine vocal physiology and details of the behaviour of urban birds, both of which we argue are consistent with the increased frequency of urban birdsong generally being a functional adjustment to noise, rather than a consequence of singing louder.

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.

Using frequency ratios to study vocal communication

Most research on animal vocal communication analyses frequency measurements on a linear scale, but the mechanisms of pitch perception and of certain aspects of vocal production are better described on a logarithmic scale, that is, as frequency ratios. Thus, for the majority of questions in vocal communication it is advisable to use log-transformed frequency, and the objective of this article is to encourage researchers to adopt this procedure. To illustrate this transition in methodology, I present two reanalyses of work on vocal communication, at the within- and among-species levels. Changing from linear to logarithmic scales yielded qualitatively identical conclusions, even in the among-species example where larger differences in absolute frequency can weaken the correlation between measurements at these two scales. These results suggest that conclusions of past work should generally be robust, at least when the absolute frequencies being compared do not diverge excessively. Results became stronger in the among-species example, suggesting that, as expected, frequency logarithms improve the ability to demonstrate biological phenomena. I hope that this discussion will motivate researchers to analyse frequency on a logarithmic scale for most research goals on vocal communication.

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.

Signalling with a cryptic trait: the regularity of barred plumage in common waxbills

Sexual signals often compromise camouflage because of their conspicuousness. Pigmentation patterns, on the contrary, aid in camouflage. It was hypothesized that a particular type of pattern—barred plumage in birds, whereby pigmented bars extend across feathers—could simultaneously signal individual quality, because disruptions of these patterns should be perceptually salient at close range and help assess plumage condition. Here we show that common waxbills (Estrilda astrild), which have extensive barred plumage, have more regular patterns as adults than as juveniles, and that adult males have more regular patterns than females. Both these differences are indicative of sexual signalling in species with conventional sex roles. More regular barred plumage was related to better body condition in adult males. Colour ornamentation traits were also related to aspects of quality, either the same as barred plumage (body condition) or a different one (good feather development), supporting both the ‘redundant message’ and the ‘multiple message’ hypotheses for the coexistence of multiple sexual signals. Although receiver responses to the regularity of barred plumage were not studied here, research on other species has shown that barred plumage can mediate social interactions. We conclude that using barred plumage as a signal of quality helps circumvent the functional compromise between camouflage and communication.

Speciation is associated with changing ornamentation rather than stronger sexual selection

Although sexual ornamentation mediates reproductive isolation, comparative evidence does not support the hypothesis that stronger sexual selection promotes speciation. Prior analyses have neglected the possibility that decreases in ornamentation may also promote speciation, such that both increases and decreases in the strength of sexual selection and associated changes in ornamentation promote speciation. To test this hypothesis, we studied color ornamentation in one of the largest and fastest avian radiations, the estrildid finches. We show that more ornamented lineages do not speciate more, even though they tend to have faster rates of ornamental evolution, whereas changes in ornamentation (i.e., increases or decreases) are associated with speciation. This indicates that divergence in sexually selected ornamentation, rather than stronger sexual selection, promotes or is otherwise associated with speciation. We also show that gregariousness and investment in reproduction are related to the elaboration of some ornamental traits, suggesting ecological influences on speciation mediated by ornamentation. We conclude that past work focusing specifically on the strength of sexual selection may have greatly underestimated the importance of sexual ornamentation for speciation.

Using Reflectance Ratios to Study Animal Coloration

Reflectance spectrophotometry is used to quantify animal coloration and compare it across individuals, populations or species. While principles of colour perception, pigment-based colour production, and some structural-based colour production, all conform to reflectance differences on a ratio scale, reflectance is usually measured on a linear scale. Processing reflectance spectra on a linear scale distorts colour information (e.g. averaging linear spectra overestimates mean brightness), and computing receiver-independent colour metrics using linear reflectance can bias results (e.g. it underestimates differences in saturation and brightness among dark colours). Working with reflectance spectra on a ratio scale obviates those issues and improves several aspects of colour analysis, from better visualization of reflectance spectra and control of measurement error, to better colour metrics.

Release from ecological constraint erases sex difference in social ornamentation

Sex differences in animal ornamentation are thought largely genetically fixed due to stronger sexual selection on males of species with conventional sex roles. But, other types of sex differences are not genetically fixed. For example, several differences in human social behavior result instead from sociocultural or economic constraints on women. Since gregarious animals use ornamentation for various social functions, perhaps some of their sex differences are, similarly to human behavior, due to social coercion or ecological constraint (their closest equivalents to human social and economic constraints, respectively). We found sex differences in ornamentation that disappear plastically in a social species with conventional sex roles. The red bill of common waxbills (Estrilda astrild) is on average more saturated in males, but in our experiment female bill color correlated with night temperature, an important energetic stressor, suggesting that sexual dichromatism disappears when ecological conditions are favorable to females. Female ornamentation may be more adversely affected by ecology because of their life history that requires balancing investment in ornamentation with maintaining reproductive condition. Manipulation of stress-related physiology (ACTH challenge) suggests that this effect was not mediated by stress mechanisms. Social coercion appears to not explain sexual dichromatism: males were not more aggressive than females, aggressiveness was not related to bill color, and manipulation of reproductive axis’ physiology (GnRH challenge, which in many species mediates aggressiveness) did not increase bill color. Our results show parallels to the plastic sex differences of humans in social animals and suggest that studying their ecological vs. social causes provides a biological backdrop for understanding the human case as well.Significance statementMany sex differences in human social behavior result from economic or sociocultural constraints on women, while sex differences in the ornamentation of animals with conventional sex roles are thought largely genetically fixed. We show that a sex difference in ornamentation—the redder bills of male than female common waxbills—disappears plastically in an animal with conventional sex roles due to, in part, changes in female ornamentation. Social coercion did not explain reduced female ornamentation: aggressiveness did not predict bill color, and males were not dominant over females. Instead, female bill color was reduced during colder weather, perhaps because females under energetic stress need to balance investment in social ornamentation vs. maintaining reproductive condition. Similarly to humans, some sex differences of gregarious animals may be due to females requiring appropriate conditions to express their full social potential.

Advancing the inference of performance in birdsong

It is appealing to integrate different acoustic traits to infer differences in performance demands among birdsongs, and to use this as a tool for investigating which roles song performance plays in communication. But inferring performance from acoustic measurements introduces a degree of interpretation that can cause disagreement. Here I give an overview of approaches to assess song performance, associated methodological issues, and ways of addressing them. I note advantages and limitations of performance metrics derived from physiological principles or from acoustic trade-offs, discuss issues with the scaling of performance metrics, and with choosing and adapting metrics to different study species and research goals. Throughout I emphasize that these metrics provide tentative assessments of performance, and that empirical results should be interpreted by comparison to alternative hypotheses.