Color as an Interspecific Badge of Status: A Comparative Test.

AbstractAnimals as diverse as cephalopods, insects, fish, and mammals signal social dominance to conspecifics to avoid costly fights. Even though between-species fights may be equally costly, the extent to which dominance signals are used between species is unknown. Here, we test the hypothesis that differences in color are associated with dominance between closely related species that aggressively interact over resources, examining between-species variation in colors that are used in within-species badges of status (black, white, and carotenoid coloration) in a comparative analysis of diverse species of birds. We found that dominant species have more black, on average, than subordinate species, particularly in regions important for aggressive signaling (face, throat, and bill). Furthermore, dominant species were more likely to have more black in comparisons in which the dominant species was similar in size or smaller than the subordinate, suggesting that black may be a more important signal when other signals of dominance (size) are missing. Carotenoid colors (i.e., red, pink, orange, and yellow) were not generally associated with dominance but may signal dominance in some taxonomic groups. White may have opposing functions: white was associated with dominance in species in which black was also associated with dominance but was associated with subordinance in species in which carotenoid-based dominance signals may be used. Overall, these results provide new evidence that colors may function broadly as signals of dominance among competing species. Such signals could help to mediate aggressive interactions among species, thereby reducing some costs of co-occurrence and facilitating coexistence in nature.

Experimental test of selection against hybridization as a driver of avian signal divergence.

Signal divergence may be pivotal in the generation and maintenance of new biodiversity by allowing closely related species to avoid some costs of co-occurrence. In birds, closely related, sympatric species are more divergent in their colour patterns than those that live apart, but the selective pressures driving this pattern remain unclear. Traditionally, signal divergence among sympatric species is thought to result from selection against hybridization, but broad evidence is lacking. Here, we conducted field experiments on naïve birds using spectrometer-matched, painted 3D-printed models to test whether selection against hybridization drives colour pattern divergence in the genus Poecile. To address selection for male colour pattern divergence without the influence of learning or the evolution of female discrimination in sympatry, we simulated secondary contact between Poecile species, and conducted mate choice experiments on naïve, allopatric females. We found that female black-capped chickadees (Poecile atricapillus) are equally likely to perform copulation solicitation displays to sympatric and allopatric heterospecific congeners when they are paired with conspecifics, but exhibit a strong preference for less divergent males when presented with paired heterospecific congeners. These results suggest that increased colour pattern divergence among sympatric species can reduce the likelihood of mixed mating in some contexts, and therefore should be favoured by selection against hybridization.

Aggressive signaling among competing species of birds.

Aggressive interactions help individuals to gain access to and defend resources, but they can be costly, leading to increased predation risk, injury, or death. Signals involving sounds and color can allow birds to avoid the costs of intraspecific aggressive encounters, but we know less about agonistic signaling between species, where fights can be frequent and just as costly. Here, we review photographic and video evidence of aggressive interactions among species of birds (N = 337 interactions documenting the aggressive signals of 164 different bird species from 120 genera, 50 families, and 24 orders) to document how individuals signal in aggressive encounters among species, and explore whether these visual signals are similar to those used in aggressive encounters with conspecifics. Despite the diversity of birds examined, most aggressively signaling birds displayed weapons (bills, talons, wings) used in fighting and placed these weapons closest to their heterospecific opponent when signaling. Most species oriented their bodies and heads forward with their bills pointing towards their heterospecific opponent, often highlighting their face, throat, mouth, and bill. Many birds also opened their wings and/or tails, increasing their apparent size in displays, consistent with the importance of body size in determining behavioral dominance among species. Aggressive postures were often similar across species and taxonomic families. Exceptions included Accipitridae and Falconidae, which often highlighted their talons in the air, Columbidae, which often highlighted their underwings from the side, and Trochilidae, which often hovered upright in the air and pointed their fanned tail downward. Most species highlighted bright carotenoid-based colors in their signals, but highlighted colors varied across species and often involved multiple colors in combination (e.g., black, white, and carotenoid-based colors). Finally, birds tended to use the same visual signals in aggressive encounters with heterospecifics that they use in aggressive encounters with conspecifics, suggesting that selection from aggressive interactions may act on the same signaling traits regardless of competitor identity.

Experimental tests of selection against heterospecific aggression as a driver of avian colour pattern divergence.

Signal divergence is thought to reduce the costs of co-occurrence for closely related species and may thereby be important in the generation and maintenance of new biodiversity. In birds, closely related, sympatric species are more divergent in their colour patterns than those that live apart, but the selective pressures driving sympatric divergence in colour pattern are not well-understood. Here, we conducted field experiments on naïve birds using spectrometer-matched, painted, 3D-printed models to test whether selection against heterospecific aggression might drive colour pattern divergence in the genus Poecile. We found that territorial male black-capped chickadees (P. atricapillus) are equally likely to attack sympatric and allopatric congeners, and wintering flocks are equally likely to visit feeders occupied by sympatric and allopatric congeners, despite sympatric congeners being more divergent in colour pattern. These results suggest that either the concerted evolution of additional traits (e.g. discrimination), or interactions in sympatry that promote learning, is required if colour pattern divergence among sympatric species is to reduce heterospecific aggression. Alternatively, colour pattern divergence among sympatric species may be caused by other selective pressures, such as selection against hybridization or habitat partitioning and secondary signal adaptation.

Size-dependent costs of migration: Migrant bird species are subordinate to residents, but only at small body sizes.

Migrant species are commonly thought to be poor competitors in aggressive interactions with resident species. However, no studies have tested whether this relationship is widespread. Here, we compare the behavioural dominance of closely related species of migratory and nonmigratory birds, testing whether migrants are consistently subordinate to resident species in aggressive contests. We compiled published behavioural dominance data involving migrant and resident congeners, gathering additional data on the body mass and migratory distance of each species. Focal species included a diverse array of birds (28 taxonomic families, 12 orders) from around the world. We found that migrant species are usually subordinate to resident species, but that this relationship disappears at larger body sizes. For smaller birds (<500 g), resident species were behaviourally dominant in 83%-88% of comparisons; for larger birds (>500 g), resident species were dominant in only 25%-30% of comparisons. The relative difference in body mass best predicted dominance relationships among species, with larger species dominant in 80%-84% of comparisons. When migrant and resident masses were equal, however, resident species were still more likely to be dominant in smaller birds, suggesting that other factors may also contribute to the subordinate status of migrants. Overall, our results suggest that in smaller species, the evolution of migration is associated with lighter weights and other traits that compromise the competitive abilities of migrants relative to residents. In contrast, larger species appear able to evolve migration without compromising their size or competitive abilities in aggressive contests, suggesting size-dependent constraints on the evolution of migration.

A comparison of genomic islands of differentiation across three young avian species pairs.

Detailed evaluations of genomic variation between sister species often reveal distinct chromosomal regions of high relative differentiation (i.e., "islands of differentiation" in FST ), but there is much debate regarding the causes of this pattern. We briefly review the prominent models of genomic islands of differentiation and compare patterns of genomic differentiation in three closely related pairs of New World warblers with the goal of evaluating support for the four models. Each pair (MacGillivray's/mourning warblers; Townsend's/black-throated green warblers; and Audubon's/myrtle warblers) consists of forms that were likely separated in western and eastern North American refugia during cycles of Pleistocene glaciations and have now come into contact in western Canada, where each forms a narrow hybrid zone. We show strong differences between pairs in their patterns of genomic heterogeneity in FST , suggesting differing selective forces and/or differing genomic responses to similar selective forces among the three pairs. Across most of the genome, levels of within-group nucleotide diversity (πWithin ) are almost as large as levels of between-group nucleotide distance (πBetween ) within each pair, suggesting recent common ancestry and/or gene flow. In two pairs, a pattern of the FST peaks having low πBetween suggests that selective sweeps spread between geographically differentiated groups, followed by local differentiation. This "sweep-before-differentiation" model is consistent with signatures of gene flow within the yellow-rumped warbler species complex. These findings add to our growing understanding of speciation as a complex process that can involve phases of adaptive introgression among partially differentiated populations.

Phenotypic divergence during speciation is inversely associated with differences in seasonal migration.

Differences in seasonal migration might promote reproductive isolation and differentiation by causing populations in migratory divides to arrive on the breeding grounds at different times and/or produce hybrids that take inferior migratory routes. We examined this question by quantifying divergence in song, colour, and morphology between sister pairs of North American migratory birds. We predicted that apparent rates of phenotypic differentiation would differ between pairs that do and do not form migratory divides. Consistent with this prediction, results from mixed effects models and Ornstein-Uhlenbeck models of evolution showed different rates of divergence between these groups; surprisingly, differentiation was greater among non-divide pairs. We interpret this finding as a result of variable rates of population blending and fusion between partially diverged forms. Ancient pairs of populations that subsequently fused are now observed as a single form, whereas those that did not fuse are observable as pairs and included in our study. We propose that fusion of two populations is more likely to occur when they have similar migratory routes and little other phenotypic differentiation that would cause reproductive isolation. By contrast, pairs with migratory divides are more likely to remain reproductively isolated, even when differing little in other phenotypic traits. These findings suggest that migratory differences may be one among several isolating barriers that prevent divergent populations from fusing and thereby increase the likelihood that they will continue differentiating as distinct species.