Ecological speciation in Darwin's finches: Ghosts of finches future.

The theory of ecological speciation posits that adaptive divergence among incipient species raises incidental barriers to reproduction, thus catalyzing the emergence of new species. In this study, we conducted an experimental test of this theory in Galápagos finches, a clade in which beaks and mating songs are mechanistically linked. We forecasted the acoustic structure of songs for a set of possible evolutionary futures (successive droughts spurring increasingly large beaks) and, in a field assay, presented resulting song simulations to territorial males. We found that responses to songs dropped off after six simulated drought events, to degrees roughly comparable to drops in response to songs that diverged through cultural drift and acoustic adaptation. Our results support, in Darwin's finches, the feasibility and mechanistic bases of an ecological speciation hypothesis.

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.

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.

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.

Vocal output predicts territory quality in a Neotropical songbird.

Females who choose highly ornamented mates may gain resources that improve offspring production and survival. Studies have focused on the relationship between male quality and the complexity of sexual ornaments; however, less is known of the communicative content of courtship displays, and whether they indicate the quality of resources males can provide to mates. Here, we used blue-black grassquits (Volatinia jacarina) to test the relationship between male display attributes and territory quality, measured as food availability. Our main hypothesis was that territory quality would be better predicted by dynamic displays than by static ornaments. During four breeding seasons in central Brazil, we quantified display song attributes (output and consistency) and the timing of nuptial molt. We measured territorial seed density, body condition, and ectoparasite infestation. We found a positive relationship between song output and territory seed density, suggesting this attribute provides a reliable indicator of territory quality. However, the timing of molt was unrelated to territory quality. Additionally, no other male attribute was associated with seed density. The link between song output and territory quality might reflect variation in male condition in response to territorial resources, or extra time males on higher quality territories have to invest in territorial defense. This article is part of a Special Issue entitled: Neotropical Behaviour.

Exploring possible human influences on the evolution of Darwin's finches.

Humans are an increasingly common influence on the evolution of natural populations. Potential arenas of influence include altered evolutionary trajectories within populations and modifications of the process of divergence among populations. We consider this second arena in the medium ground finch (Geospiza fortis) on Santa Cruz Island, Galápagos, Ecuador. Our study compared the G. fortis population at a relatively undisturbed site, El Garrapatero, to the population at a severely disturbed site, Academy Bay, which is immediately adjacent to the town of Puerto Ayora. The El Garrapatero population currently shows beak size bimodality that is tied to assortative mating and disruptive selection, whereas the Academy Bay population was historically bimodal but has lost this property in conjunction with a dramatic increase in local human population density. We here evaluate potential ecological-adaptive drivers of the differences in modality by quantifying relationships between morphology (beak and head dimensions), functional performance (bite force), and environmental characteristics (diet). Our main finding is that associations among these variables are generally weaker at Academy Bay than at El Garrapatero, possibly because novel foods are used at the former site irrespective of individual morphology and performance. These results are consistent with the hypothesis that the rugged adaptive landscapes promoting and maintaining diversification in nature can be smoothed by human activities, thus hindering ongoing adaptive radiation.

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.

Acoustic discrimination of sympatric morphs in Darwin's finches: a behavioural mechanism for assortative mating?

Populations with multiple morphological or behavioural types provide unique opportunities for studying the causes and consequences of evolutionary diversification. A population of the medium ground finch (Geospiza fortis) at El Garrapatero on Santa Cruz Island, Galápagos, features two beak size morphs. These morphs produce acoustically distinctive songs, are subject to disruptive selection and mate assortatively by morph. The main goal of the present study was to assess whether finches from this population are able to use song as a cue for morph discrimination. A secondary goal of this study was to evaluate whether birds from this population discriminate songs of their own locality versus another St Cruz locality, Borrero Bay, approximately 24 km to the NW. I presented territorial males with playback of songs of their own morph, of the other morph, and of males from Borrero Bay. Males responded more strongly to same-morph than to other-morph playbacks, showing significantly shorter latencies to flight, higher flight rates and closer approaches to the playback speaker. By contrast, I found only minor effects of locality on responsiveness. Evidence for morph discrimination via acoustic cues supports the hypothesis that song can serve as a behavioural mechanism for assortative mating and sympatric evolutionary divergence.

Divergence with gene flow as facilitated by ecological differences: within-island variation in Darwin's finches.

Divergence and speciation can sometimes proceed in the face of, and even be enhanced by, ongoing gene flow. We here study divergence with gene flow in Darwin's finches, focusing on the role of ecological/adaptive differences in maintaining/promoting divergence and reproductive isolation. To this end, we survey allelic variation at 10 microsatellite loci for 989 medium ground finches (Geospiza fortis) on Santa Cruz Island, Galápagos. We find only small genetic differences among G. fortis from different sites. We instead find noteworthy genetic differences associated with beak. Moreover, G. fortis at the site with the greatest divergence in beak size also showed the greatest divergence at neutral markers; i.e. the lowest gene flow. Finally, morphological and genetic differentiation between the G. fortis beak-size morphs was intermediate to that between G. fortis and its smaller (Geospiza fuliginosa) and larger (Geospiza magnirostris) congeners. We conclude that ecological differences associated with beak size (i.e. foraging) influence patterns of gene flow within G. fortis on a single island, providing additional support for ecological speciation in the face of gene flow. Patterns of genetic similarity within and between species also suggest that interspecific hybridization might contribute to the formation of beak-size morphs within G. fortis.

Mechanical stress, fracture risk and beak evolution in Darwin's ground finches (Geospiza).

Darwin's finches have radiated from a common ancestor into 14 descendent species, each specializing on distinct food resources and evolving divergent beak forms. Beak morphology in the ground finches (Geospiza) has been shown to evolve via natural selection in response to variation in food type, food availability and interspecific competition for food. From a mechanical perspective, however, beak size and shape are only indirectly related to birds' abilities to crack seeds, and beak form is hypothesized to evolve mainly under selection for fracture avoidance. Here, we test the fracture-avoidance hypothesis using finite-element modelling. We find that across species, mechanical loading is similar and approaches reported values of bone strength, thus suggesting pervasive selection on fracture avoidance. Additionally, deep and wide beaks are better suited for dissipating stress than are more elongate beaks when scaled to common sizes and loadings. Our results illustrate that deep and wide beaks in ground finches enable reduction of areas with high stress and peak stress magnitudes, allowing birds to crack hard seeds while limiting the risk of beak failure. These results may explain strong selection on beak depth and width in natural populations of Darwin's finches.

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.

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.

Amazonian ecology: tributaries enhance the diversity of electric fishes.

Neotropical rivers support a diverse array of endemic taxa, including electric fishes of the order Gymnotiformes. A comprehensive survey of the main channels of the Amazon River and its major tributaries (>2000-kilometer transect) yielded 43 electric fish species. Biogeographical analyses suggest that local mainstem electric fish diversity is enhanced by tributaries. Mainstem species richness tends to increase downstream of tributary confluences, and species composition is most similar between tributaries and adjacent downstream mainstem locations. These findings support a "nodal" or heterogeneous model of riverine community organization across a particularly extensive and diverse geographical region.

Vocal mechanics in Darwin's finches: correlation of beak gape and song frequency.

Recent studies of vocal mechanics in songbirds have identified a functional role for the beak in sound production. The vocal tract (trachea and beak) filters harmonic overtones from sounds produced by the syrinx, and birds can fine-tune vocal tract resonance properties through changes in beak gape. In this study, we examine patterns of beak gape during song production in seven species of Darwin's finches of the Galápagos Islands. Our principal goals were to characterize the relationship between beak gape and vocal frequency during song production and to explore the possible influence therein of diversity in beak morphology and body size. Birds were audio and video recorded (at 30 frames s(-1)) as they sang in the field, and 164 song sequences were analyzed. We found that song frequency regressed significantly and positively on beak gape for 38 of 56 individuals and for all seven species examined. This finding provides broad support for a resonance model of vocal tract function in Darwin's finches. Comparison among species revealed significant variation in regression y-intercept values. Body size correlated negatively with y-intercept values, although not at a statistically significant level. We failed to detect variation in regression slopes among finch species, although the regression slopes of Darwin's finch and two North American sparrow species were found to differ. Analysis within one species (Geospiza fortis) revealed significant inter-individual variation in regression parameters; these parameters did not correlate with song frequency features or plumage scores. Our results suggest that patterns of beak use during song production were conserved during the Darwin's finch adaptive radiation, despite the evolution of substantial variation in beak morphology and body size.