Temporally varying disruptive selection in the medium ground finch (Geospiza fortis).

Disruptive natural selection within populations exploiting different resources is considered to be a major driver of adaptive radiation and the production of biodiversity. Fitness functions, which describe the relationships between trait variation and fitness, can help to illuminate how this disruptive selection leads to population differentiation. However, a single fitness function represents only a particular selection regime over a single specified time period (often a single season or a year), and therefore might not capture longer-term dynamics. Here, we build a series of annual fitness functions that quantify the relationships between phenotype and apparent survival. These functions are based on a 9-year mark-recapture dataset of over 600 medium ground finches (Geospiza fortis) within a population bimodal for beak size. We then relate changes in the shape of these functions to climate variables. We find that disruptive selection between small and large beak morphotypes, as reported previously for 2 years, is present throughout the study period, but that the intensity of this selection varies in association with the harshness of environment. In particular, we find that disruptive selection was strongest when precipitation was high during the dry season of the previous year. Our results shed light on climatic factors associated with disruptive selection in Darwin's finches, and highlight the role of temporally varying fitness functions in modulating the extent of population differentiation.

Genomic variation at the tips of the adaptive radiation of Darwin's finches.

Adaptive radiation unfolds as selection acts on the genetic variation underlying functional traits. The nature of this variation can be revealed by studying the tips of an ongoing adaptive radiation. We studied genomic variation at the tips of the Darwin's finch radiation; specifically focusing on polymorphism within, and variation among, three sympatric species of the genus Geospiza. Using restriction site-associated DNA (RAD-seq), we characterized 32 569 single-nucleotide polymorphisms (SNPs), from which 11 outlier SNPs for beak and body size were uncovered by a genomewide association study (GWAS). Principal component analysis revealed that these 11 SNPs formed four statistically linked groups. Stepwise regression then revealed that the first PC score, which included 6 of the 11 top SNPs, explained over 80% of the variation in beak size, suggesting that selection on these traits influences multiple correlated loci. The two SNPs most strongly associated with beak size were near genes associated with beak morphology across deeper branches of the radiation: delta-like 1 homologue (DLK1) and high-mobility group AT-hook 2 (HMGA2). Our results suggest that (i) key adaptive traits are associated with a small fraction of the genome (11 of 32 569 SNPs), (ii) SNPs linked to the candidate genes are dispersed throughout the genome (on several chromosomes), and (iii) micro- and macro-evolutionary variation (roots and tips of the radiation) involve some shared and some unique genomic regions.

Uneven sampling and the analysis of vocal performance constraints.

Studies of trilled vocalizations provide a premiere illustration of how performance constraints shape the evolution of mating displays. In trill production, vocal tract mechanics impose a trade-off between syllable repetition rate and frequency bandwidth, with the trade-off most pronounced at higher values of both parameters. Available evidence suggests that trills that simultaneously maximize both traits are more threatening to males or more attractive to females, consistent with a history of sexual selection favoring high-performance trills. Here, we identify a sampling limitation that confounds the detection and description of performance trade-offs. We reassess 70 data sets (from 26 published studies) and show that sampling limitations afflict 63 of these to some degree. Traditional upper-bound regression, which does not control for sampling limitations, detects performance trade-offs in 33 data sets; yet when sampling limitations are controlled, performance trade-offs are detected in only 15. Sampling limitations therefore confound more than half of all performance trade-offs reported using the traditional method. An alternative method that circumvents this sampling limitation, which we explore here, is quantile regression. Our goal is not to question the presence of mechanical trade-offs on trill production but rather to reconsider how these trade-offs can be detected and characterized from acoustic data.

Team of rivals: alliance formation in territorial songbirds is predicted by vocal signal structure.

Cooperation and conflict are regarded as diametric extremes of animal social behaviour, yet the two may intersect under rare circumstances. We here report that territorial competitors in a common North American songbird species, the chipping sparrow (Spizella passerina), sometimes form temporary coalitions in the presence of simulated territorial intruders. Moreover, analysis of birds' vocal mating signals (songs) reveals that coalitions occur nearly exclusively under specific triadic relationships, in which vocal performances of allies and simulated intruders exceed those of residents. Our results provide the first evidence that animals like chipping sparrows rely on precise assessments of mating signal features, as well as relative comparisons of signal properties among multiple animals in communication networks, when deciding when and with whom to form temporary alliances against a backdrop of competition and rivalry.

Escalation of aggressive vocal signals: a sequential playback study.

Rival conspecifics often produce stereotyped sequences of signals as agonistic interactions escalate. Successive signals in sequence are thought to convey increasingly pronounced levels of aggressive motivation. Here, we propose and test a model of aggressive escalation in black-throated blue warblers, presenting subjects with two sequential and increasingly elevated levels of threat. From a speaker outside the territorial boundary, we initiated an interaction (low-threat level), and from a second speaker inside the territory, accompanied by a taxidermic mount, we subsequently simulated a territorial intrusion (escalated threat level). Our two main predictions were that signalling behaviours in response to low-threat boundary playback would predict signalling responses to the escalated within-territory threat, and that these latter signalling behaviours would in turn reliably predict attack. We find clear support for both predictions: (i) specific song types (type II songs) produced early in the simulated interaction, in response to boundary playback, predicted later use of low-amplitude 'soft' song, in response to within-territory playback; and (ii) soft song, in turn, predicted attack of the mount. Unexpectedly, use of the early-stage signal (type II song) itself did not predict attack, despite its apparent role in aggressive escalation. This raises the intriguing question of whether type II song can actually be considered a reliable aggressive signal. Overall, our results provide new empirical insights into how songbirds may use progressive vocal signalling to convey increasing levels of threat.

Responses to song playback vary with the vocal performance of both signal senders and receivers.

Mating signals of many animal species are difficult to produce and thus should indicate signaler quality. Growing evidence suggests that receivers modulate their behaviour in response to signals with varying performance levels, although little is known about if and how responses are affected by receiver attributes. To explore this topic we conducted two experiments with swamp sparrows, Melospiza georgiana, in which we challenged territorial males with playback of songs with trill rates that were natural, digitally reduced, or digitally elevated (control-, low- and high-performance stimuli, respectively). In our first experiment, we found that males responded more aggressively to control songs than to low-performance stimuli, that low-performance stimuli with the most severe trill-rate reductions elicited the weakest aggressive responses, and that the subjects' own trill rates predicted aggressive responses. In our second experiment, we found that male responses to high-performance stimuli varied significantly, in ways predicted by two factors: the degree to which we had elevated stimulus performance levels of high-performance stimuli, and subjects' own vocal performance levels. Specifically, males were less aggressive towards stimuli for which we had elevated performance levels to higher degrees, and subject males with higher vocal performances themselves responded more aggressively. These findings together offer a novel illustration of how responses to aggressive signals may rely not just on signal attributes, but also on attributes of responding animals themselves.

The fitness landscape of a community of Darwin's finches.

Divergent natural selection should lead to adaptive radiation-that is, the rapid evolution of phenotypic and ecological diversity originating from a single clade. The drivers of adaptive radiation have often been conceptualized through the concept of "adaptive landscapes," yet formal empirical estimates of adaptive landscapes for natural adaptive radiations have proven elusive. Here, we use a 17-year dataset of Darwin's ground finches (Geospiza spp.) at an intensively studied site on Santa Cruz (Galápagos) to estimate individual apparent lifespan in relation to beak traits. We use these estimates to model a multi-species fitness landscape, which we also convert to a formal adaptive landscape. We then assess the correspondence between estimated fitness peaks and observed phenotypes for each of five phenotypic modes (G. fuliginosa, G. fortis [small and large morphotypes], G. magnirostris, and G. scandens). The fitness and adaptive landscapes show 5 and 4 peaks, respectively, and, as expected, the adaptive landscape was smoother than the fitness landscape. Each of the five phenotypic modes appeared reasonably close to the corresponding fitness peak, yet interesting deviations were also documented and examined. By estimating adaptive landscapes in an ongoing adaptive radiation, our study demonstrates their utility as a quantitative tool for exploring and predicting adaptive radiation.

Structural tissue organization in the beak of Java and Darwin's finches.

Birds are well known for occupying diverse feeding niches, and for having evolved diverse beak morphologies associated with dietary specialization. Birds that feed on hard seeds typically possess beaks that are both deep and wide, presumably because of selection for fracture avoidance, as suggested by prior studies. It follows then that birds that eat seeds of different size and hardness should vary in one or more aspects of beak morphology, including the histological organization of the rhamphotheca, the cellular interface that binds the rhamphotheca to the bone, and the organization of trabeculae in the beak. To explore this expectation we here investigate tissue organization in the rhamphotheca of the Java finch, a large granivorous bird, and describe interspecific differences in the trabecular organization of the beak across 11 species of Darwin's finches. We identify specializations in multiple layers of the horny beak, with the dermis anchored to the bone by Sharpey's fibers in those regions that are subjected to high stresses during biting. Moreover, the rhamphotheca is characterized by a tight dermo-epidermal junction through interdigitations of these two tissues. Herbst corpuscles are observed in high density in the dermis of the lateral aspect of the beak as observed in other birds. Finally, the trabecular organization of the beak in Darwin's finches appears most variable in regions involved most in food manipulation, with the density of trabeculae in the beak generally mirroring loading regimes imposed by different feeding habits and beak use in this clade.

Ecology and evolution of bird sounds.

Birds are among nature's most social animals. They are renowned for their group migrations, their cooperative foraging, their communal roosting, their synchronous breeding aggregations, their precise parent-offspring interactions, their coordinated group defenses and their intricate territorial and courtship rituals. In these and other contexts, and indeed in most moments of their lives, birds' capacities to navigate complex social demands and relationships can tip the balance between health or sickness, between reproductive success or failure, between life or death. It is thus no surprise that birds have evolved sophisticated systems for mediating social interactions. Foremost among these are communication signals, most evident in birds as songs, calls, color patterns and postural displays. These and other communication signals can transmit information about a signalers' status, motivations and possible future actions, for sensory and cognitive processing by signal receivers. In general, signals provide benefits for both signal senders and receivers. Consider the bright spring plumage of a male wood warbler who has established a breeding territory. The male's plumage pattern benefits him by signaling his 'ownership' of his territory, which can help him attract potential mates and preempt conflict with potential rivals. His plumage pattern also benefits his intended audiences: it informs females about the signaler's potential as a mate, and it informs other males about the degree of threat they might face were they to attempt a territory take-over. Communication signals are, in essence, a glue that maintains the cohesion of bird societies, and a currency that mediates sophisticated relationships within.

The terroir of the finch: How spatial and temporal variation shapes phenotypic traits in DARWIN'S finches.

The term terroir is used in viticulture to emphasize how the biotic and abiotic characteristics of a local site influence grape physiology and thus the properties of wine. In ecology and evolution, such terroir (i.e., the effect of space or "site") is expected to play an important role in shaping phenotypic traits. Just how important is the pure spatial effect of terroir (e.g., differences between sites that persist across years) in comparison to temporal variation (e.g., differences between years that persist across sites), and the interaction between space and time (e.g., differences between sites change across years)? We answer this question by analyzing beak and body traits of 4388 medium ground finches (Geospiza fortis) collected across 10 years at three locations in Galápagos. Analyses of variance indicated that phenotypic variation was mostly explained by site for beak size (η 2 = 0.42) and body size (η 2 = 0.43), with a smaller contribution for beak shape (η 2 = 0.05) and body shape (η 2 = 0.12), but still higher compared to year and site-by-year effects. As such, the effect of terroir seems to be very strong in Darwin's finches, notwithstanding the oft-emphasized interannual variation. However, these results changed dramatically when we excluded data from Daphne Major, indicating that the strong effect of terroir was mostly driven by that particular population. These phenotypic results were largely paralleled in analyses of environmental variables (rainfall and vegetation indices) expected to shape terroir in this system. These findings affirm the evolutionary importance of terroir, while also revealing its dependence on other factors, such as geographical isolation.

Ontogeny of the cranial skeleton in a Darwin's finch (Geospiza fortis).

Darwin's finches are a model system in ecological and evolutionary research, but surprisingly little is known about their skull morphology and development. Indeed, only the early beak development and external variation in adult beak shape has been studied. Understanding the development of the skull from embryo up to the adult is important to gain insights into how selection acts upon, and drives, variation in beak shape. Here, we provide a detailed description of the skeletal development of the skull in the medium ground finch (Geospiza fortis). Although the ossification sequence of the cranial elements is broadly similar to that observed for other birds, some differences can be observed. Unexpectedly, our data show that large changes in skull shape take place between the nestling and the juvenile phases. The reorientation of the beak, the orbit and the formation of well-developed processes and cristae suggest that these changes are likely related to the use of the beak after leaving the nest. This suggests that the active use of the jaw muscles during seed cracking plays an important role in shaping the adult skull morphology and may be driving some of the intra-specific variation observed in species such as G. fortis. Investigating the development of the jaw muscles and their interaction with the observed ossification and formation of the skull and lower jaw would allow further insights into the ecology and evolution of beak morphology in Darwin's finches.

The head of the finch: the anatomy of the feeding system in two species of finches (Geospiza fortis and Padda oryzivora).

Despite the large number of studies devoted to the evolution of beak shape in Darwin's finches, surprisingly little is known about the morphology of the skull and jaw musculature in these birds. Moreover, it remains currently unclear whether Darwin's finches are unusual in their cranial morphology compared with other seed-cracking birds. Here, we provide a detailed description of the morphology of the cranial system in the medium ground finch (Geospiza fortis) and compare it with that of another seed-cracking bird of similar overall size and appearance, the Java finch (Padda oryzivora). Our data show an overall similarity in beak size and cranial morphology. Yet, differences in the jaw adductor size and corresponding attachments to the cranium and mandible are prominent, with the medium ground finch having much more robust jaw-closing muscles. This is reflected in differences in bite forces, with the medium ground finch biting much harder than the Java finch. These data suggest similarities in the evolution of the feeding system in birds specializing in the cracking of hard seeds, but also show the uniqueness of the cranial morphology and bite force of the medium ground finch compared with other seed-cracking birds.

Hormonal and behavioral correlates of morphological variation in an Amazonian electric fish (Sternarchogiton nattereri: Apteronotidae).

The weakly electric fish from the main channel of the Amazon river, Sternarchogiton nattereri, offers a striking case of morphological variation. Females and most males are toothless, or present only few minute teeth on the mandible, whereas some males exhibit exaggerated, spike-like teeth that project externally from the snout and chin. Androgens are known to influence the expression of sexually dimorphic traits, and might be involved in tooth emergence. In this study we assess the relationship in S. nattereri between morphological variation, 11 ketotestosterone (11-KT) and testosterone (T). We also examine relationships of morphology and androgen levels with electric organ discharge (EOD) frequency, reproductive condition, and seasonality. Our main finding is that male morph categories differed significantly in plasma concentrations of 11-KT, with toothed males showing higher levels of 11-KT than toothless males. By contrast, we did not detect statistical differences in T levels among male morph categories. Reproductive condition, as measured by gonadosomatic indexes (GSI), differed across two sample years, increased as the season progressed, and was higher in toothed males than in non-toothed males. EOD frequency was higher in toothed males than in either toothless males or females. Taken together, our findings suggest that S. nattereri male sexual characters are regulated by 11-KT levels, and that both morphology and androgens interact with reproductive condition and EOD frequency in ways that vary within and across reproductive seasons.

Persistence of song types in Darwin's finches, Geospiza fortis, over four decades.

Learned bird songs evolve via cultural evolution, with song patterns transmitted across generations by imitative learning. In Darwin's finches of the Galápagos Islands, males learn songs from their fathers, and song types can be maintained across multiple generations. However, little is known about the time frame over which specific song types are preserved, in the face of copy errors and corresponding modifications to song structure. Here we investigate cultural evolution in songs of male Geospiza fortis, at Academy Bay, Santa Cruz Island, comparing songs recorded in 1961 by R. Bowman (20 individuals) to those recorded in 1999 by J. Podos (16 individuals). For each individual, we characterized four timing and six frequency parameters, and assessed inter-individual variation in song structure using multivariate analysis. Several 1961 song types persisted into 1999, some with remarkable fidelity. Variation among song types was extensive during both years, and we detected no changes in 10 vocal parameters across the sampling period. These results illustrate temporal continuity in a culturally acquired trait, and raise questions about mechanisms that promote stability in song structure.

Disruptive selection in a bimodal population of Darwin's finches.

A key part of the ecological theory of adaptive radiation is disruptive selection during periods of sympatry. Some insight into this process might be gained by studying populations that are bimodal for dual-context traits, i.e. those showing adaptive divergence and also contributing to reproductive isolation. A population meeting these criteria is the medium ground finch (Geospiza fortis) of El Garrapatero, Santa Cruz Island, Galápagos. We examined patterns of selection in this population by relating individual beak sizes to interannual recaptures during a prolonged drought. Supporting the theory, disruptive selection was strong between the two beak size modes. We also found some evidence of selection against individuals with the largest and smallest beak sizes, perhaps owing to competition with other species or to gaps in the underlying resource distribution. Selection may thus simultaneously maintain the current bimodality while also constraining further divergence. Spatial and temporal variation in G. fortis bimodality suggests a dynamic tug of war among factors such as selection and assortative mating, which may alternatively promote or constrain divergence during adaptive radiation.

Extremely loud mating songs at close range in white bellbirds.

Sexual selection in many animal species favors the evolution of elaborate courtship traits. Such traits might help signalers convey, and receivers discern, information about signaler quality; or they might be favored by perceptual or aesthetic preferences for elaborateness or beauty [1-3]. Under either scenario we expect sexual trait elaboration to be countered by proximate constraints rooted in animals' morphology, physiology and phylogenetic history [3,4]. During expeditions to a montane rainforest in the Brazilian Amazon, we obtained amplitude-calibrated measures of mating songs in two species of cotingas, the white bellbird (Procnias albus) and the screaming piha (Lipaugus vociferans). The screaming piha sings the loudest songs of any passerine bird previously documented [5]. However, we find that white bellbirds are >9 dB louder, and thus achieve roughly triple the sound pressure levels of pihas. Mechanical constraints on amplitude, and thus limits on the reach of sexual selection, are revealed by trade-offs between maximal sound pressure and song duration. We find that song amplitude in bellbirds is context-dependent: when a female was on the display perch, a male bellbird sang only his louder song type, swiveling his body mid-song to face the female head on. We know of no other species in which such high-amplitude vocal signals are directed to receivers in such close proximity. We propose that bellbird females balance an interest in sampling males at close range with a need to protect themselves from hearing damage.

Urbanization erodes niche segregation in Darwin's finches.

Urbanization is influencing patterns of biological evolution in ways that are only beginning to be explored. One potential effect of urbanization is in modifying ecological resource distributions that underlie niche differences and that thus promote and maintain species diversification. Few studies have assessed such modifications, or their potential evolutionary consequences, in the context of ongoing adaptive radiation. We study this effect in Darwin's finches on the Galápagos Islands, by quantifying feeding preferences and diet niche partitioning across sites with different degrees of urbanization. We found higher finch density in urban sites and that feeding preferences and diets at urban sites skew heavily toward human food items. Furthermore, we show that finches at urban sites appear to be accustomed to the presence of people, compared with birds at sites with few people. In addition, we found that human behavior via the tendency to feed birds at non-urban but tourist sites is likely an important driver of finch preferences for human foods. Site differences in diet and feeding behavior have resulted in larger niche breadth within finch species and wider niche overlap between species at the urban sites. Both factors effectively minimize niche differences that would otherwise facilitate interspecies coexistence. These findings suggest that both human behavior and ongoing urbanization in Galápagos are starting to erode ecological differences that promote and maintain adaptive radiation in Darwin's finches. Smoothing of adaptive landscapes underlying diversification represents a potentially important yet underappreciated consequence of urbanization. Overall, our findings accentuate the fragility of the initial stages of adaptive radiation in Darwin's finches and raise concerns about the fate of the Galápagos ecosystems in the face of increasing urbanization.

Animal Behavior: Song Learning out of the Box.

Our understanding of songbird song learning is derived mainly from two approaches: observations in the field and experiments in the laboratory. A clever new study combines elements of both and highlights how exposure to song can catalyze imitative learning.

Reproductive isolation of sympatric morphs in a population of Darwin's finches.

Recent research on speciation has identified a central role for ecological divergence, which can initiate speciation when (i) subsets of a species or population evolve to specialize on different ecological resources and (ii) the resulting phenotypic modes become reproductively isolated. Empirical evidence for these two processes working in conjunction, particularly during the early stages of divergence, has been limited. We recently described a population of the medium ground finch, Geospiza fortis, that features large and small beak morphs with relatively few intermediates. As in other Darwin's finches of the Galápagos Islands, these morphs presumably diverged in response to variation in local food availability and inter- or intraspecific competition. We here demonstrate that the two morphs show strong positive assortative pairing, a pattern that holds over three breeding seasons and during both dry and wet conditions. We also document restrictions on gene flow between the morphs, as revealed by genetic variation at 10 microsatellite loci. Our results provide strong support for the central role of ecology during the early stages of adaptive radiation.