Daniel T. Baldassarre

GENOMIC AND MORPHOLOGICAL ANALYSIS OF A SEMIPERMEABLE AVIAN HYBRID ZONE SUGGESTS ASYMMETRICAL INTROGRESSION OF A SEXUAL SIGNAL

Hybrid zones are geographic regions where differentiated taxa meet and potentially exchange genes. Increasingly, genomic analyses have demonstrated that many hybrid zones are semipermeable boundaries across which introgression is highly variable. In some cases, certain alleles penetrate across the hybrid zone in only one direction, recombining into the alternate genome. We investigated this phenomenon using genomic (genotyping‐by‐sequencing) and morphological (plumage reflectance spectrophotometry) analyses of the hybrid zone between two subspecies of the red‐backed fairy‐wren (Malurus melanocephalus) that differ conspicuously in a sexual signal, male back plumage color. Geographic cline analyses revealed a highly variable pattern of differential introgression, with many narrow coincident clines combined with several significantly wider clines, suggesting that the hybrid zone is a semipermeable tension zone. The plumage cline was shifted significantly into the genomic background of the orange subspecies, consistent with sexual selection driving asymmetrical introgression of red plumage alleles across the hybrid zone. This interpretation is supported by previous experimental work demonstrating an extra‐pair mating advantage for red males, but the role of genetic dominance in driving this pattern remains unclear. This study highlights the potential for sexual selection to erode taxonomic boundaries and promote gene flow, particularly at an intermediate stage of divergence.

Experimental evidence that extra-pair mating drives asymmetrical introgression of a sexual trait

Theory suggests that traits under positive selection may introgress asymmetrically across a hybrid zone, potentially driven by sexual selection. Two subspecies of the red-backed fairy-wren (Malurus melanocephalus) differ primarily in a sexual signal used in mate choice—red versus orange male back plumage colour—but phylogeographic analyses suggest asymmetrical introgression of red plumage into the genetic background of the orange subspecies. We hypothesized that this asymmetrical introgression may be facilitated by sexual selection if red males have a mating advantage over orange males. We tested this hypothesis with correlational data and a plumage manipulation experiment where we reddened the back plumage of a subset of orange males to mimic males of the red subspecies. There was no correlational evidence of a mating advantage to naturally redder males in this population. Experimentally reddened males sired a similar amount of within-pair young and lost paternity at the same rate as orange males, but they sired significantly more extra-pair young, leading to substantially higher total reproductive success. Thus, we conclude that sexual selection via extra-pair mating is a likely mechanism responsible for the asymmetrical introgression of plumage colour in this system, and is potentially driven by a sensory bias for the red plumage signal.

Interaction between female mating preferences and predation may explain the maintenance of rare males in the pentamorphic fish Poecilia parae

Variation in mating preferences coupled with selective predation may allow for the maintenance of alternative mating strategies. Males of the South American live‐bearing fish Poecilia parae fall in one of five discrete morphs: red, yellow, blue, stripe‐coloured tail (parae) and female mimic (immaculata). Field surveys indicate that the red and yellow morphs are the rarest and that their rarity is consistent across years. We explored the role of variable female mating preference and selective predation by visual predators in explaining the rarity of red and yellow males, and more generally, the maintenance of this extreme colour polymorphism. We presented wild‐caught P. parae females and Aequidens tetramerus, the most common cichlid predator, with the five male colour morphs in separate trials to determine mating and prey preferences, respectively. We found that a large proportion of females shared a strong preference for the rare carotenoid‐based red and yellow males, but a distinct group also preferred the blue and parae morphs. The cichlid predator strongly preferred red and yellow males as prey. Together, these results suggest that the interaction between premating sexual selection favouring and predation acting against the red and yellow morphs may explain their rarity in the wild. The trade‐off between sexual and natural selection, accompanied by variation in female mating preferences, may therefore facilitate the maintenance of the striking colour polymorphism in P. parae.

Differential rates of phenotypic introgression are associated with male behavioral responses to multiple signals.

Sexual selection on multiple signals may lead to differential rates of signal introgression across hybrid zones if some signals contribute to reproductive isolation but others facilitate gene flow. Competition among males is one powerful form of sexual selection, but male behavioral responses to multiple traits have not been considered in a system where traits have introgressed differentially. Using playbacks, mounts, and a reciprocal experimental design, we tested the hypothesis that male responses to song and plumage in two subspecies of red‐backed fairy‐wren (Malurus melanocephalus) explain patterns of differential signal introgression (song has not introgressed, whereas plumage color has introgressed asymmetrically). We found that males of both subspecies discriminated symmetrically between subspecies’ songs at a long range, but at a close range, we found that aggression was equal for both subspecies’ plumage and songs. Taken together, our results suggest that male behavioral responses hinder the introgression of song, but allow for the observed asymmetrical introgression of plumage. Our results highlight how behavioral responses are a key component of signal evolution when recently divergent taxa come together, and how differential responses to multiple signals may lead to differential signal introgression and novel trait combinations.

Variation in song system anatomy and androgen levels does not correspond to song characteristics in a tropical songbird

Variation in song structure and song production of birds are thought to relate to variation of both androgen levels and neural nuclei in the song system, as typically these nuclei are larger in males than in females, vary in size among males and are sensitive to steroid hormones. We investigated the relationships among song and note structure, singing rate, androgen levels and the sizes of two song nuclei, the higher vocal centre (HVC) and the robust nucleus of the arcopallium (RA) in male and female red-backed fairy-wrens, Malurus melanocephalus. Males of this duetting species express three discrete reproductive phenotypes that differ in plumage colour and behaviour. Although HVC and RA structure differed between the sexes, there were no sex differences in note structure and complexity of songs, although females differed from some male types in song rate and frequency characteristics. Both auxiliary males and females had significantly lower androgen levels than the two breeding male phenotypes. Male reproductive phenotypes had similar song characteristics and HVC and RA structure, but differed in androgen levels. Sexes and male phenotypes varied in song rate, but these differences did not correspond to differences in androgen levels. Thus, sex differences in song nuclei anatomy and androgen levels were not associated with differences in song structure and singing rate; and, the differences in androgen levels among male phenotypes were not reflected in differences in singing rate, song structure or the song nuclei. We conclude that, similar to other recent findings, the sexes of the red-backed fairy-wren can produce similar song and express similar singing behaviour despite differences in song system structure and circulating androgen levels; singing and song system anatomy appear not to be part of the suite of traits associated with differences in androgen levels in male red-backed fairy-wrens.

Multiple hypotheses explain variation in extra-pair paternity at different levels in a single bird family

Extra‐pair paternity (EPP), where offspring are sired by a male other than the social male, varies enormously both within and among species. Trying to explain this variation has proved difficult because the majority of the interspecific variation is phylogenetically based. Ideally, variation in EPP should be investigated in closely related species, but clades with sufficient variation are rare. We present a comprehensive multifactorial test to explain variation in EPP among individuals in 20 populations of nine species over 89 years from a single bird family (Maluridae). Females had higher EPP in the presence of more helpers, more neighbours or if paired incestuously. Furthermore, higher EPP occurred in years with many incestuous pairs, populations with many helpers and species with high male density or in which males provide less care. Altogether, these variables accounted for 48% of the total and 89% of the interspecific and interpopulation variation in EPP. These findings indicate why consistent patterns in EPP have been so challenging to detect and suggest that a single predictor is unlikely to account for the enormous variation in EPP across levels of analysis. Nevertheless, it also shows that existing hypotheses can explain the variation in EPP well and that the density of males in particular is a good predictor to explain variation in EPP among species when a large part of the confounding effect of phylogeny is excluded.

The couple that sings together stays together: duetting, aggression and extra-pair paternity in a promiscuous bird species

When individuals mate outside the pair bond, males should employ behaviours such as aggression or vocal displays (e.g. duetting) that help assure paternity of the offspring they care for. We tested whether male paternity was associated with aggression or duetting in the red-backed fairy-wren, a species exhibiting high rates of extra-pair paternity. During simulated territorial intrusions, aggression and duetting were variable among and repeatable within males, suggesting behavioural consistency of individuals. Males with quicker and stronger duet responses were cuckolded less often than males with slower and weaker responses. In contrast, physical aggression was not correlated with male paternity. These results suggest that either acoustic mate guarding or male–female vocal negotiations via duetting lead to increased paternity assurance, whereas physical aggression does not.

Subtle benefits of cooperation to breeding males of the Red-backed Fairywren

ABSTRACT Cooperative breeding is a phenomenon whereby breeding and nonbreeding individuals collectively provision young. Nonbreeding group members (“helpers”) may gain indirect and/or direct fitness benefits by breeding in a group, but there has been conflicting evidence regarding the benefits to breeders. In fact, the presence of helpers may sometimes be detrimental to aspects of breeder fitness. For example, in some species of the chiefly Australian genus Malurus, breeding males with helpers have lower within-pair paternity than do males without helpers. Additionally, indirect benefits to breeding males are often limited by low relatedness to their helpers due to high extrapair paternity rates, and helpers often appear to have minimal impact on breeder reproductive success. However, the presence of helpers may allow breeding males to shift their behaviors from guarding and provisioning young to alternative behaviors that affect other components of fitness, such as extraterritory forays (which might increase extrapair mating success) and self-maintenance (which might increase survival). We investigated these possibilities in the facultatively cooperative Red-backed Fairywren (Malurus melanocephalus). Males with helpers spent significantly less time engaging in guarding behaviors and provisioning of young than did those without helpers, but there was no difference in the frequency of extrapair forays nor the number of young sired by males with vs. without helpers. Additionally, the decreased investment in nesting behaviors did not result in consistently higher survival, but may have increased survival in some years. Overall, the results of this study did not suggest any strong direct fitness benefits to breeding males, which may indicate that the costs of retaining helpers are negligible relative to the indirect benefits of helping a potentially related male.