The evolution of immune defense and song complexity in birds

Abstract There are three main hypotheses that explain how the evolution of parasite virulence could be linked to the evolution of secondary sexual traits, such as bird song. First, as Hamilton and Zuk proposed a role for parasites in sexual selection, female preference for healthy males in heavily parasitized species may result in extravagant trait expression. Second, a reverse causal mechanism may act, if sexual selection affects the coevolutionary dynamics of host-parasite interactions per se by selecting for increased virulence. Third, the immuno-suppressive effects of ornamentation by testosterone or limited resources may lead to increased susceptibility to parasites in species with elaborate songs. Assuming a coevolutionary relationship between parasite virulence and host investment in immune defense we used measures of immune function and song complexity to test these hypotheses in a comparative study of passerine birds. Under the first two hypotheses we predicted avian song complexity to be positively related to immune defense among species, whereas this relationship was expected to be negative if immuno-suppression was at work. We found that adult T-cell mediated immune response and the relative size of the bursa of Fabricius were independently positively correlated with a measure of song complexity, even when potentially confounding variables were held constant. Nestling T-cell response was not related to song complexity, probably reflecting age-dependent selective pressures on host immune defense. Our results are consistent with the hypotheses that predict a positive relationship between song complexity and immune function, thus indicating a role for parasites in sexual selection. Different components of the immune system may have been independently involved in this process.     

Fitness correlates of song repertoire size in free-living song sparrows (Melospiza melodia)

Models of sexual selection propose that exaggerated secondary sexual ornaments indicate a male's own fitness and the fitness of his offspring. These hypotheses have rarely been thoroughly tested in free-living individuals because overall fitness, as opposed to fitness components, is difficult to measure. We used 20 years of data from song sparrows (Melospiza melodia) inhabiting Mandarte Island, British Columbia, Canada, to test whether a male's song repertoire size, a secondary sexual trait, predicted overall measures of male or offspring fitness. Males with larger song repertoires contributed more independent and recruited offspring, and independent and recruited grandoffspring, to Mandarte's population. This was because these males lived longer and reared a greater proportion of hatched chicks to independence from parental care, not because females mated to males with larger repertoires laid or hatched more eggs. Furthermore, independent offspring of males with larger repertoires were more likely to recruit and then to leave more grandoffspring than were offspring of males with small repertoires. Although we cannot distinguish whether observed fitness variation reflected genetic or environmental effects on males or their offspring, these data suggest that female song sparrows would gain immediate and intergenerational fitness benefits by pairing with males with large song repertoires.     

Element repertoire: change and development with age in Whitethroat Sylvia communis song

Song repertoires are often important determining factors in sexual selection. In several species, older males have larger repertoires than 1-year-old males. The development of large song repertoires by an individual is, however, poorly understood. We studied song element repertoire changes in five individual male Whitethroats Sylvia communis sampled as 1- and 2-year olds. These males increased the size of their element repertoire between their first and second year, but song length and number of different elements per song did not change. On average, 44.3% of the song elements in the first-year repertoire were also found in the second-year repertoire. Elements shared between years were found earlier in the songs and tended to occur in sequences. Sequences of shared elements also seemed to be conserved between years. The study suggests that the song element repertoire of the second year is partly based on the first-year repertoire, which may explain why large song repertoires are mainly expressed by males at least 2 years of age. It would appear, therefore, that song element repertoire size could be a reliable signal of male age.     

Song repertoire size varies with HVC volume and is indicative of male quality in song sparrows (Melospiza melodia)

Complex birdsong is a classic example of a sexually selected ornamental trait. In many species, females prefer males with large song repertoires, possibly because repertoire size is limited by the size of song control nuclei which reflect developmental success. We investigated whether song repertoire size was indicative of brain area and male quality in song sparrows (Melospiza melodia) by determining if repertoire size was related to the volume of song control nucleus HVC, as well as several morphological, immunological and genetic indices of quality. We found that males with large repertoires had larger HVCs and were in better body condition. They also had lower heterophil to lymphocyte ratios, indicating less physiological stress and a robust immune system as measured by the number of lymphocytes per red blood cell. Song repertoire size also tended to increase with neutral-locus genetic diversity, as assessed by mean d2, but was not related to internal relatedness. Our results suggest several mechanisms that might explain the finding of a recent study that song sparrows with large song repertoires have higher lifetime fitness.     

Is female preference for male repertoires due to sensory bias?

There are several possible explanations for the female preference for male repertoires in birds. These males are older, and have better territories; thus there are functional reasons for females to prefer these males. However, there is an alternative explanation; females may habituate less quickly to song repertoires than single songs. I tested whether females have a non-functional, sensory bias for male song repertoires, by testing female preference for a repertoire in zebra finches (Taenopygia guttata), a species in which males possess a single stereotyped song. Females chose between a male repertoire of four different phrases created from the song phrase of one individual and that of one of those phrases repeated four times (natural zebra finch song). Females were also given a choice between the above repertoire and a song made from the phrases of four related males (''family'' stimulus). I tested female preference by training females to press a button for presentation of a song stimulus, and counting the number of button presses. Females preferred the song repertoire to a single phrase song, and did not differentiate between the repertoire and song phrases from four males. Evidence from the Estrildidae indicates that having a single song is the ancestral state for zebra finches, so the preference is not ancestral.     

Secondary sexual ornamentation and non-additive genetic benefits of female mate choice

Ornamental secondary sexual traits are hypothesized to evolve in response to directional mating preferences for more ornamented mates. Such mating preferences may themselves evolve partly because ornamentation indicates an individual's additive genetic quality (good genes). While mate choice can also confer non-additive genetic benefits (compatible genes), the identity of the most 'compatible' mate is assumed to depend on the choosy individual's own genotype. It is therefore unclear how choice for non-additive genetic benefits could contribute to directional mating preferences and consequently the evolution of ornamentation. In free-living song sparrows (Melospiza melodia), individual males varied in their kinship with the female population. Furthermore, a male's song repertoire size, a secondary sexual trait, was negatively correlated with kinship such that males with larger repertoires were less closely related to the female population. After excluding close relatives as potential mates, individual females were on average less closely related to males with larger repertoires. Therefore, female song sparrows expressing directional preferences for males with larger repertoires would on average acquire relatively unrelated mates and produce relatively outbred offspring. Such non-additive genetic fitness benefits of directional mating preferences, which may reflect genetic dominance variance expressed in structured populations, should be incorporated into genetic models of sexual selection.     

Elevating perceived predation risk modifies the relationship between parental effort and song complexity in the song sparrow Melospiza melodia

Adult‐directed predation risk elevates costs of parental care, and may modify relationships between sexually selected ornaments and parental effort by accentuating the tradeoff between survival and parental investment. We assessed multiple hypotheses regarding the relationship between maternal effort, paternal effort, and the sexually selected trait of male song complexity in the song sparrow Melospiza melodia. Further, we explored whether experimentally elevating perceived adult‐directed predation risk near nests affected these relationships. We quantified two dimensions of song complexity: song repertoire size and residual syllable number (the relative number of syllables for a given song repertoire size). Under elevated perceived predation risk, but not in the absence of the predator stimuli, females mated to males with higher residual syllable number displayed higher nestling provisioning rates and performed a greater proportion of nestling provisioning trips. In other words, elevating perceived predation risk induced a pattern of maternal investment consistent with differential allocation. In contrast, under elevated perceived predation risk, only, females performed a lesser proportion of provisioning trips when mated to males with large song repertoire sizes. Further, consistent with the good parent hypothesis, males with large song repertoire sizes displayed lower latencies to return to the nest, independent of the predator stimuli. Results suggest that residual syllable number may reflect some aspect of male genetic quality, such that females are more willing to maintain maternal effort while facing heightened predation risk. On the other hand, females may gain paternal benefits when mated to males with large song repertoires. Our study supports the hypothesis that increased costs of parental care associated with predation risk may induce relationships between sexually selected traits and parental behavior, which may increase the strength of sexual selection. Additionally, results suggest that different aspects of song complexity may fulfill non‐equivalent signaling roles.     

Song Sharing in Neighboring and Non-Neighboring Thrush Nightingales (Luscinia luscinia) and its Implications for Communication

In many passerines, males have repertoires of different songs of which some songs are often shared with other males. Sharing of song repertoires among males can provide insights into the context in which songs were acquired and on the role of song repertoires in inter- and intrasexual communication. Here we studied repertoire sharing in male territorial thrush nightingales ( Luscinia luscinia ). We compared male vocal repertoires of the basic song components, full songs, and the sequencing of songs in a bout. The results show that males differed significantly in the size of their song repertoires but not in the size of the repertoire of basic song components. Moreover, they shared almost all (80%) the repertoire of song components but only 30% of their song types. Neighboring males shared significantly more song types than did non-neighboring males but interestingly they did not share more basic song components than non-neighboring males. These results show that the repertoire of basic song components is under much less sexual selection than the size of song repertoires. Sharing of song repertoires among neighbors presumably results from repertoire conversion over time and from males returning to their territories in the following season. Repertoire sharing then can be an indicator of territory tenure and thus it can be important in repelling rivals and in female choice.     

Sexual Differences in the Responses of Captive Great Reed Warblers (Acrocephalus arundinaceus) to Variation in Song Structure and Repertoire Size

The function and evolution of repertoires in songbirds is still not clearly understood. This study involves the great reed warbler Acrocephalus arundinaceus and playback of recorded song to both captive males and females under controlled laboratory conditions. Females were implanted with oestradiol and the copulation solicitation display used as an index of sexual response. Males were not implanted and crest-raising used as an index of aggressive response. Two types of songs were used (short and long) and two sizes of repertoire (high and low). Females only responded to long songs, and responded significantly more to high than low repertoires. It was concluded that long songs have a sexual function and that high repertoires are the result of intersexual selection through female choice. Males responded to short and long songs, but did not discriminate between high and low repertoires. Adding a live male to the experiment made no difference to female responses but males responded significantly more. When field studies are also taken into consideration the overall conclusion is that song quality and repertoire size is particularly important in female choice, and that short songs and a male presence are more important in aggressive behaviour. Integration of both field and laboratory studies on males and females should lead to more rigorous testing of hypotheses concerning the function and evolution of bird songs.     

Nestling growth and song repertoire size in great reed warblers: evidence for song learning as an indicator mechanism in mate choice

Females of many songbird species show a preference for mating with males that have larger song repertoires, but the advantages associated with this preference are uncertain. We tested the hypothesis that song complexity can serve as an indicator of male quality because the development of the brain regions underlying song learning and production occurs when young birds typically face nutritional and other stresses, so that song reflects how well a male fared during post-hatch development. A key prediction of this hypothesis is that variation in nestling condition should correspond to variation in the adult song repertoires of individuals. We used data from a long-term study of the great reed warbler (Acrocephalus arundinaceus) to test this prediction, correlating two measures of nestling development with subsequent repertoire size of males. We found that the length of the innermost primary feather, a standard measure of development, significantly predicted first-year repertoire size. The relationship between repertoire size and body mass was nearly significant, in spite of the large variance inherent in this measure. These data support the idea that song may provide females with information about a male's response to developmental stress, which in turn is expected to correlate with indirect or direct benefits she might receive.     

Evidence of repertoire sharing and stability despite a high turnover rate in a duetting neotropical wren

In songbirds, the spatial pattern of song sharing among individuals is influenced by the song learning and dispersal strategies within each species. In birds where females and males sing and create joint acoustic displays (duets), the processes defining the patterns of song sharing become more complex as there might be different selection pressures shaping the behaviour of each sex. To provide further insight into the vocal development and the dispersal strategy of duetting tropical species, we investigated the patterns of individual and pair repertoire sharing, as well as the stability of these repertoires, in a colour-marked population of riverside wrens, Cantorchilus semibadius, located in the Osa Peninsula, Costa Rica. Using data collected over a five-year period, we found considerable variation in the sharing levels of phrase and duet type repertoires among neighbouring individuals coupled with a general decline of repertoire sharing as distance increased between birds’ territories. These results are consistent with a pattern predicted in age-restricted learners that establish preferentially near their tutors. Furthermore, we found no evidence of individuals changing their phrase type repertoires over time, including after remating events. Duet type repertoires were also stable when pairs remained together. However, we observed a surprisingly high turnover rate. When individuals remated, even though the majority of the previous duet type repertoire remained, several new duet types were included. Taken together, our findings suggest that riverside wrens might create their individual repertoires by copying their same-sex parent and neighbouring individuals before dispersal. Additionally, we speculate that even though birds were able to create new duet types after changing partners, a substantial portion of their duet type repertoire might also be copied from their parents and neighbouring pairs during the initial critical period of song learning.     

Hamilton and Zuk meet heterozygosity? Song repertoire size indicates inbreeding and immunity in song sparrows (Melospiza melodia)

Hamilton and Zuk's influential hypothesis of parasite-mediated sexual selection proposes that exaggerated secondary sexual ornaments indicate a male's addictive genetic immunity to parasites. However, genetic correlated of ornaments and immunity have rarely been explicitly identified. Evidence supporting Hamilton and Zuk's hypothesis has instead been gathered by looking for positive phenotypic correlations between ornamentation and immunity; such correlations are assumed to reflect causal, addictive relationships between these traits. We show that in a song sparrows, Melospiza melodia, male's song repertoire size, a secondary sexual trait, increased with his cell-mediated immune response (CMI) to an experimental challenge. However, this phenotypic correlation could be explained because both repertoire size and CMI declined with a male's inbreeding level. Repertoire size therefore primarily indicated a male's relative heterozygosity, a non-addictive genetic predictor of immunity. Caution may therefore be required when interpreting phenotypic correlations as support for Hamilton and Zuk's addictive model of sexual selection. However, our results suggest that female song sparrows choosing with large repertoires would on average acquire more outbred and therefore more heterozygous mates. Such genetic dominance effects on ornamentation are likely to influence evolutionary trajectories of female choice, and should be explicitly incorporated into genetic models of sexual selection.     

First-Year Common Nightingales (Luscinia megarhynchos) Have Smaller Song-Type Repertoire Sizes Than Older Males

Based on the assumptions that birdsong indicates male quality and that quality is related to age, one might expect older birds to signal their age. That is, in addition to actual body condition, at least some song features should vary with age, presumably towards more complexity. We investigated this issue by comparing repertoire sizes of free‐ranging common nightingale males in their first breeding season with those of older males. Nightingales are a good model species as they are open‐ended learners, where song acquisition is not confined to an early sensitive period of learning. Moreover, nightingales develop an extraordinarily large song‐type repertoire (approx. 180 different song types per male), and differences in repertoire size among males are pronounced. We analysed repertoire characteristics of the nocturnal song of nine nightingales in their first breeding season and compared them with the songs of nine older males. The repertoire size of older males was on average 53% larger than that of yearlings. When analysing two song categories of nightingales, whistle and non‐whistle songs separately, we found similar results. Our findings show marked differences in repertoire size between age categories, suggesting that this song feature may reflect a male's age. We discuss those mechanisms that may constrain the development of larger repertoires in first‐year males. Whether repertoire sizes are crucial for female mate choice or in vocal interactions among conspecific males remains open to further investigations.     

Trill consistency is an age-related assessment signal in banded wrens

Older males tend to have a competitive advantage over younger males in sexual selection. Therefore, it is expected that signals used in sexual selection change with age. Although song repertoire size in songbirds is often mentioned as an age-related trait, many species, including the banded wren (Thryothorus pleurostictus), do not increase their repertoires after the first year. Here, we show that banded wrens reproduce the trill notes in their songs with less variability between them (i.e. more consistently) when they grow older. In a playback experiment, we also show that banded wrens discriminate between younger and older birds based on structural aspects of their song. In a second experiment, banded wrens also respond differentially to natural songs versus songs with artificially enhanced consistency. We argue that consistency in trill note reproduction may be achieved through practice. Sexual selection in the form of male–male competition may therefore operate on a phenotypic trait, the expression of which is enhanced by practice.     

Testosterone-induced Singing in Female European Starlings (Sturnus vulgaris)

Adult female starlings (Sturnus vulgaris) were injected with testosterone in order to determine the song structures they had in memory. Those females had been caught in the wild in different geographical areas and had different ages. This hormone treatment clearly stimulated singing behaviour of females in isolation and revealed their ability to sing quite complex songs. Both categories of songs observed in males (warbling and whistles) were demonstrated and large repertoires were observed. Although the testosterone treatment may have altered the female song system and induced male-like vocalizations, it is interesting that none of the species-typic elements of male starlings was produced by the experimental females. Large changes were found in both repertoire size and composition over a year, revealing a high plasticity, even in older birds. We also found evidence that even under testosterone treatment, females do not necessarily sing all the songs they may have in memory.     

Directional Sexual Selection Cannot Explain Variation in Song Repertoire Size in the New World Blackbirds (Icterinae)

Hypotheses that song repertoire evolves by way of directional sexual selection for large repertoires were examined with a comparative study of the avian subfamily Icterinae (Passeriformes: Emberiznae). Song repertoire size varies between closely related icterine species, so phylogenetic effects cannot explain repertoire size variation. Overall, song repertoire is not associated with polygyny or with presence or absence of territoriality. Different associations of repertoire with mating system are observed in different icterine groups. Either the directional hypotheses do not apply to the evolution of song repertoire in the Icterinae, or different processes of directional sexual selection have occurred in different icterine groups.     

Singing the Popular Songs? Nightingales Share More Song Types with Their Breeding Population in Their Second Season than in Their First

Signals used in communication often change throughout an individual’s life course. For example, in many song bird species, males modify their song especially between their first and second breeding season. To address one possible reason of such modification, we investigated whether common nightingales Luscinia megarhynchos adjust their song type repertoires to sing the song types commonly occurring in their breeding population. We analysed nocturnal singing of six nightingales in their first and second breeding season and compared their repertoire composition and usage to the ‘typical’ repertoire and usage on the breeding ground (represented by seven reference birds). Songs that were maintained between the first and second season by the six focal birds occurred in most of the repertoires of the seven reference birds and were sung often. In contrast, song types that were dropped from the repertoires occurred less often in the reference birds’ repertoires and were sung less often. Furthermore, in the first year, each focal nightingale’s repertoire was less similar to the reference birds’ repertoires than in the second year. Thus, nightingales adjusted their singing towards the songs popular in the breeding grounds by keeping song types that were common and frequently sung by other individuals in their breeding area and by disposing of infrequently performed ones. This resulted in increased similarity with the population’s repertoire from the first to the second year. We discuss possible ontogenetic processes that may lead to such an adjustment and suggest an improved ability to match song types as possible adaptive value.     

Are there age-related differences in the song repertoire size of Eurasian blackbirds?

Most oscine bird species possess a repertoire of different song patterns, and repertoire size is thought to signal aspects of male quality. As age is assumed to be related to male quality in terms of experience and/or viability, repertoire size may be expected to reflect male age. Here, we investigated the relationship between repertoire size and age (yearlings or older) in Eurasian blackbirds, Turdus merula, a species with a large repertoire delivered in a highly variable manner. We found that older males tended to have larger repertoires than yearlings though the two age groups overlapped considerably. Thus, compared to other species with large repertoires, age-related differences in repertoire size seem rather small in male Eurasian blackbirds. We also compared repertoires of three individuals in two successive years (as yearlings and in the year following) and found a large element turnover. Our investigation revealed that this turnover was almost complete in the quiet terminating twitter part of the song. Such turnover may allow a young bird to adjust his repertoire to his neighbours?? repertoires, which could be useful for song matching interactions.     

Multilevel selection and neighbourhood effects from individual to metapopulation in a wild passerine

Multilevel selection has rarely been studied in the ecological context of animal populations, in which neighbourhood effects range from competition among territorial neighbours to source-sink effects among local populations. By studying a Dupont's lark Chersophilus duponti metapopulation, we analyze neighbourhood effects mediated by song repertoires on fitness components at the individual level (life-span) and population level (growth rate). As a sexual/aggressive signal with strong effects on fitness, birdsong creates an opportunity for group selection via neighbour interactions, but may also have population-wide effects by conveying information on habitat suitability to dispersing individuals. Within populations, we found a disruptive pattern of selection at the individual level and an opposite, stabilizing pattern at the group level. Males singing the most complex songs had the longest life-span, but individuals with the poorest repertoires lived longer than 'average' males, a finding that likely reflects two male strategies with respect to fitness and sexual trait expression. Individuals from groups with intermediate repertoires had the longest life-span, likely benefitting from conspecific signalling to attract females up to the detrimental spread of competitive interactions in groups with superior vocal skills. Within the metapopulation selection was directional but again followed opposite patterns at the two levels: Populations had the highest growth rate when inhabiting local patches with complex repertoires surrounded by patches with simple repertoires. Here the song may impact metapopulation dynamics by guiding prospecting individuals towards populations advertising habitat quality. Two fitness components linked to viability were therefore influenced by the properties of the group, and birdsong was the target of selection, contributing to linking social/sexual processes at the local scale with regional population dynamics.     

SONG POPULATIONS AND DISPERSAL IN STEELBLUE AND PURPLE WIDOWFINCHES

Payne, R. B. 1985. Song populations and dispersal in Steelblue and Purple Widowfinches. Ostrich 56:135-146.

Songs of Steelblue Widowfinches Vidua chalybeata were recorded over eight years at Lochinvar National Park, Zambia. Neighbouring males share their song-type repertoires. Individual birds changed the structural details of all song types in their repertoire from year to year, and over 4–5 years the songs accumulated changes so that a song type could scarcely be recognized as the same. A few males in addition switched their song repertoires when they dispersed from one song population to another, or when their old neighbours disappeared and new neighbouring males sang a different song repertoire. Individual marked adult birds moved from one song neighbourhood to another. Purple Widowfinches had a similar song behaviour but only one song dialect was found in the study area.

An estimate of the proportion of immigrants was made from the proportion of birds with songs unlike their neighbours, and from birds that had a mixed song repertoire or that switched their song repertoires. Song populations were sampled at several localities in the Transvaal, Botswana, Zambia, Kenya, Tanzania, Cameroon, and Nigeria. An overall minimal estimate of dispersal between song neighbourhoods was 18 %. The incidence of observed dispersal and the movements indicated by the song differences among local widowfinches were considerable and more than sufficient to prevent genetic isoloation and differentiation of local song populations.