Dense sampling of bird diversity increases power of comparative genomics.

Whole-genome sequencing projects are increasingly populating the tree of life and characterizing biodiversity1-4. Sparse taxon sampling has previously been proposed to confound phylogenetic inference5, and captures only a fraction of the genomic diversity. Here we report a substantial step towards the dense representation of avian phylogenetic and molecular diversity, by analysing 363 genomes from 92.4% of bird families-including 267 newly sequenced genomes produced for phase II of the Bird 10,000 Genomes (B10K) Project. We use this comparative genome dataset in combination with a pipeline that leverages a reference-free whole-genome alignment to identify orthologous regions in greater numbers than has previously been possible and to recognize genomic novelties in particular bird lineages. The densely sampled alignment provides a single-base-pair map of selection, has more than doubled the fraction of bases that are confidently predicted to be under conservation and reveals extensive patterns of weak selection in predominantly non-coding DNA. Our results demonstrate that increasing the diversity of genomes used in comparative studies can reveal more shared and lineage-specific variation, and improve the investigation of genomic characteristics. We anticipate that this genomic resource will offer new perspectives on evolutionary processes in cross-species comparative analyses and assist in efforts to conserve species.

Inclusive fitness theory and eusociality.

Arising from M. A. Nowak, C. E. Tarnita & E. O. Wilson 466, 1057-1062 (2010); Nowak et al. reply. Nowak et al. argue that inclusive fitness theory has been of little value in explaining the natural world, and that it has led to negligible progress in explaining the evolution of eusociality. However, we believe that their arguments are based upon a misunderstanding of evolutionary theory and a misrepresentation of the empirical literature. We will focus our comments on three general issues.

Limited variation in visual sensitivity among bowerbird species suggests that there is no link between spectral tuning and variation in display colouration.

Variation in visual spectral tuning has evolved in concert with signal colour in some taxa, but there is limited evidence of this pattern in birds. To further investigate this possibility, we compared spectral sensitivity among bowerbird species that occupy different visual habitats and are highly diverged in plumage and decoration colour displays, which are important in mate choice and possibly reproductive isolation. Microspectrophotometry of violet-, short-, medium- and long-wavelength-sensitive cones revealed no significant interspecific variation in visual pigment peak spectral absorbance values that ranged between 404-410, 454, 503-511 and 558-568 nm, respectively. Mean cut-off wavelength values for C-, Y-, R- and P-type coloured oil droplets were 418-441, 508-523, 558-573 and 412-503 nm, respectively, with values at longer wavelengths in ventral compared with dorsal retina cones. Low ocular media mid-wavelength transmission values (340-352 nm) suggest that bowerbirds may represent a transitional stage in the evolution from the ancestral violet-sensitive- to the derived ultraviolet-sensitive-type short-wavelength-sensitive-1-based visual system found in younger passerine lineages. Sequence data obtained for rod opsin and four cone opsin genes were identical at key tuning sites, except for an interspecific leucine-52-alanine polymorphism in the short-wavelength-sensitive 2 opsin. There was no obvious relationship between relative proportions of cone classes and either visual habitat or display colour. Overall, we detected little interspecific variation in bowerbird spectral sensitivity and no association between sensitivity and display diversity, which is consistent with the general trend among avian taxa.

Aerobic capacity in wild satin bowerbirds: repeatability and effects of age, sex and condition.

Individual variation in aerobic capacity has been extensively studied, especially with respect to condition, maturity or pathogen infection, and to gain insights into mechanistic foundations of performance. However, its relationship to mate competition is less well understood, particularly for animals in natural habitats. We examined aerobic capacity [maximum rate of O2 consumption (VO2,max) in forced exercise] in wild satin bowerbirds, an Australian passerine with a non-resource based mating system and strong intermale sexual competition. We tested for repeatability of mass and VO2,max, differences among age and sex classes, and effects of several condition indices. In adult males, we examined interactions between aerobic performance and bower ownership (required for male mating success). There was significant repeatability of mass and VO2,max within and between years, but between-year repeatability was lower than within-year repeatability. VO2,max varied with an overall scaling to mass(0.791), but most variance in VO2,max was not explained by mass. Indicators of condition (tarsus and wing length asymmetry, the ratio of tarsus length to mass) were not correlated to VO2,max. Ectoparasite counts were weakly correlated to VO2,max across all age-sex classes but not within any class. Adult males, the cohort with the most intense levels of mating competition, had higher VO2,max than juvenile birds or adult females. However, there was no difference between the VO2,max of bower-owning males and that of males not known to hold bowers. Thus one major factor determining male reproductive success was not correlated to aerobic performance.

Variable female preferences drive complex male displays.

Complexity in male sexual displays is widely appreciated but diversity in female mate choice has received little attention. Males of many species have sexual displays composed of multiple display traits, and females are thought to use these different traits in mate choice. Models of multiple display trait evolution suggest that these traits provide females with different kinds of information in different stages of the mate choice process, or function as redundant signals to improve the accuracy of mate assessment. We suggest that complex male displays might also arise because of variation in female preferences for particular male display traits. The causes of female preference variation have received little attention, and the role of preference variation in shaping complex male displays is unclear. Here we show that in satin bowerbirds (Ptilonorhynchus violaceus) female mate choice is a multistage process, where females of different ages use different male display traits in successive stages. Age- and stage-specific female preferences may contribute to explaining the widespread occurrence of multifaceted male displays.

Evolution of colorful display.

How the displays of bowerbirds have evolved has attracted widespread interest. Endler et al. (2005) analyzed color use in display in a subset of bowerbird species and generalized their results to all bowerbirds. Here we discuss problems with their analysis that calls into question their conclusions. For example, they state that bowerbirds do not use decorations that match their background, but this is not supported by their results. They reconstruct historical patterns of sexual dimorphism in plumage display using questionable methodology. The high lability of these display traits makes these reconstructions unreliable and, using accepted methods and acknowledging the lability problem, we were unable to support their conclusions. Their claim that plumage differences between sympatric species are due to character displacement is not supported by the available data. Their focus is on visual contrast as the cause for display color and we offer additional hypotheses that may contribute to explaining color use. We support studies of spectral analysis of display traits but urge greater care in using this information to reach conclusions about how colorful displays have evolved.

Multiple male traits interact: attractive bower decorations facilitate attractive behavioural displays in satin bowerbirds.

Sexually selected male courtship displays often involve multiple behavioural and physical traits, but little is known about the function of different traits in mate choice. Here, we examine female courtship behaviours to learn how male traits interact to influence female mating decisions. In satin bowerbirds (Ptilonorhynchus violaceus), successful males give highly aggressive, intense behavioural displays without startling females. Males do this by modulating their displays in response to female crouching, which signals the display intensity that females will tolerate without being startled. Females typically visit multiple males for multiple courtships before choosing a mate, and females show differing tolerance for intense displays during their first courtship with each male. We test three hypotheses that may explain this: (i) familiarity with the courting male; (ii) the order of the courtship in mate-searching; and (iii) the attractiveness of the courting male. We found that females are more tolerant of intense displays during first courtships with attractive males; this increased female tolerance may allow attractive males to give higher intensity courtship displays that further enhance their attractiveness. We then examined why this is so, finding evidence that females are less likely to be startled by males with better physical displays (bower decorations), and this reduced startling then contributes to male courtship success. This role of physical displays in facilitating behavioural displays suggests a novel mechanism by which multiple physical and behavioural traits may influence female choice.

Comment on "Illusions promote mating success in great bowerbirds".

Kelley and Endler (Reports, 20 January 2012, p. 335) claim that male great bowerbirds construct a visual illusion, using display object gradients, that affects mating success. We argue that they provide inadequate statistical support for their hypothesis, inappropriately exclude important data, and do not consider other display traits that explain mating success. We propose a more plausible alternative hypothesis to explain display object patterns.

Plumage based classification of the bowerbird genus Sericulus evaluated using a multi-gene, multi-genome analysis.

Past classifications of taxa within the bowerbird genus Sericulus (family: Ptilonorhynchidae) conflict since the discovery of hybrids identified though male plumage characteristics. We use molecular data to help define species within this genus, and by estimating a phylogeny, test for lability in the evolution of male plumage patterns. Because this genus includes the most brightly colored bowerbird species, and is hypothesized to be the basal genus of the avenue building bowerbird clade, the organization of the four taxa within this genus is especially important in understanding how bowerbird plumage coloration evolved. Analyses of two mitochondrial and six nuclear gene regions confirm the basal placement of Sericulus in the avenue building bowerbirds and Sericulus monophyly, and suggests the Australian S. chrysocephalus is the basal Sericulus species. Our analysis additionally supports the existence of three New Guinea Sericulus species, contrary to some previous plumage based classifications, as they are genetically equidistant from each other. Molecular and geographic data of New Guinea are consistent suggesting a series of speciation events starting approximately 3.7-4.3MYA leading to four extant Sericulus species. The absence of resolution within the New Guinea species precludes any statements of trait lability, but does suggest that traits under high selection pressures may not accurately indicate species level distinctions within this genus.

Female preferences drive the evolution of mimetic accuracy in male sexual displays.

Males in many bird species mimic the vocalizations of other species during sexual displays, but the evolutionary and functional significance of interspecific vocal mimicry is unclear. Here we use spectrographic cross-correlation to compare mimetic calls produced by male satin bowerbirds (Ptilonorhynchus violaceus) in courtship with calls from several model species. We show that the accuracy of vocal mimicry and the number of model species mimicked are both independently related to male mating success. Multivariate analyses revealed that these mimetic traits were better predictors of male mating success than other male display traits previously shown to be important for male mating success. We suggest that preference-driven mimetic accuracy may be a widespread occurrence, and that mimetic accuracy may provide females with important information about male quality. Our findings support an alternative hypothesis to help explain a common element of male sexual displays.

Male displays adjusted to female's response.

Models of sexual selection generally assume that behavioural courtship displays reflect intrinsic male qualities such as condition, and that males display with maximum intensity to attract females to mate. Here we use robotic females in a field experiment to demonstrate that male satin bowerbirds (Ptilonorhynchus violaceus) do not always display at maximum intensity - rather, successful males modulate their displays in response to signals from females. Our results indicate that sexual selection may favour those males that can produce intense displays but which know how to modify these according to the female response.