Every inch a finch: a commentary on Grant (1993) ‘Hybridization of Darwin's finches on Isla Daphne Major,Galapagos’

One of the most familiar features of the natural world is that most animals and plants fall into distinct categories known as species. The attempt to understand the nature of species and the origin of new species was the enterprise that drove the early development of evolutionary biology and has continued to be a major focus of research. Individuals belonging to the same species usually share a distinctive appearance and way of life, and they can mate together successfully and produce viable offspring. New species may evolve, therefore, either through ecological divergence or through sexual isolation. The balance between these processes will depend on the extent of hybridization, especially in the early stages of divergence. Detecting and measuring hybridization in natural populations, however, requires intensive, long-term field programmes that are seldom undertaken, leaving a gap in our understanding of species formation. The finch community of a small, isolated island in the Galapagos provided an opportunity to discover how frequently hybridization takes place between closely related species in a pristine location, and Peter Grant''s paper, published in Philosophical Transactions B in 1993, reports the observations that he and his collaborators made during the first 20 years of what is now one of the classical studies of evolution in action. This commentary was written to celebrate the 350th anniversary of the journal Philosophical Transactions of the Royal Society.     

Morphological differentiation in Carduelis finches: Adaptive vs. constraint models

In this study we show that morphological diversification in the avian genus Carduelis (Carduelinae) has to a large extent been conservative. Using multivariate methods, we found only minor deviations from the common (ancestral) body-plan. In particular, variation in bill morphology was found to be more conservative than variation in other parts of the body. We argue that constraint models of population differentiation can successfully account for the variation in bill morphology in this genus, but are less successful in accounting for variation in other traits. This can be interpreted as a result of long-term overall stabilizing selection for a certain bill morphology which is related to the way the birds open seeds. A trait combination that is adaptive on the evolutionary time scale may thus act as a constraint on changes in bill morphology on the microevolutionary scale. We conclude that the most parsimonious explanation for low divergence in bill morphology in this genus is that all species have retained the ancestral bill morphology. This may mean that each species chooses its environment rather than being moulded by it. This argument seems to apply to bill morphology, but other traits studied in this genus appear to have evolved in a less constrained fashion. A new index of morphometric integration is introduced to describe covariance structures.     

Interactive effects of environmental stress and inbreeding on reproductive traits in a wild bird population

1. Conservation biologists are concerned about the interactive effects of environmental stress and inbreeding because such interactions could affect the dynamics and extinction risk of small and isolated populations, but few studies have tested for these interactions in nature. 2. We used data from the long-term population study of song sparrows Melospiza melodia on Mandarte Island to examine the joint effects of inbreeding and environmental stress on four fitness traits that are known to be affected by the inbreeding level of adult birds: hatching success, laying date, male mating success and fledgling survival. 3. We found that inbreeding depression interacted with environmental stress to reduce hatching success in the nests of inbred females during periods of rain. 4. For laying date, we found equivocal support for an interaction between parental inbreeding and environmental stress. In this case, however, inbred females experienced less inbreeding depression in more stressful, cooler years. 5. For two other traits, we found no evidence that the strength of inbreeding depression varied with environmental stress. First, mated males fathered fewer nests per season if inbred or if the ratio of males to females in the population was high, but inbreeding depression did not depend on sex ratio. Second, fledglings survived poorly during rainy periods and if their father was inbred, but the effects of paternal inbreeding and rain did not interact. 6. Thus, even for a single species, interactions between the inbreeding level and environmental stress may not occur in all traits affected by inbreeding depression, and interactions that do occur will not always act synergistically to further decrease fitness.     

A developing paradigm for the development of bird beaks

Some adaptive radiations are notable for extreme interspecific diversification in one or a few adult traits. How and why have trait differences evolved? Natural and sexual selection often provide answers to the question of why. An answer to the question of how is to be found in the genetic control of the phenotypic traits, especially in the early stages of development, when interspecific differences first become expressed. Recent studies of the molecular genetic control of beak development in Darwin's finches have shown that a signalling molecule (BMP4) plays a key role in the development of large and deep beaks. Expression of this molecule occurs earlier (heterochrony) and at higher levels in species with deep beaks compared with species with more pointed beaks. The implication of this finding is that variation in the regulation of one or a few genes that are expressed early could be the source of evolutionarily significant variation that is subject to natural selection in speciation and adaptive radiation. This view is reinforced by parallel findings with the same signalling molecule in the development of jaw morphology in cichlid fish of the Great Lakes of Africa. Further research into regulatory mechanisms is to be expected, as well as extension to other examples of radiation such as honeycreepers in Hawaii and Anolis lizards in the Caribbean. © 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 88 , 17–22.     

Birds adjust acoustic directionality to beam their antipredator calls to predators and conspecifics

Animals in many vertebrate species vocalize in response to predators, but it is often unclear whether these antipredator calls function to communicate with predators, conspecifics or both. We evaluated the function of antipredator calls in 10 species of passerines by measuring the acoustic directionality of these calls in response to experimental presentations of a model predator. Acoustic directionality quantifies the radiation pattern of vocalizations and may provide evidence about the receiver of these calls. We predicted that antipredator calls would have a lower directionality if they function to communicate with surrounding conspecifics, and a higher directionality and aimed at the receiver if they function to communicate with the predator. Our results support both of these functions. Overall, the birds produce antipredator calls that have a relatively low directionality, suggesting that the calls radiate in many directions to alert conspecifics. However, birds in some species increase the directionality of their calls when facing the predator. They can even direct their calls towards the predator when facing lateral to it—effectively vocalizing sideways towards the predator. These results suggest that antipredator calls in some species are used to communicate both to conspecifics and to predators, and that birds adjust the directionality of their calls with remarkable sophistication according to the context in which they are used.     

SEX CHROMOSOME LINKAGE OF MATE PREFERENCE AND COLOR SIGNAL MAINTAINS ASSORTATIVE MATING BETWEEN INTERBREEDING FINCH MORPHS

Assortative mating is a key aspect in the speciation process because it is important for both initial divergence and maintenance of distinct species. However, it remains a challenge to explain how assortative mating evolves when diverging populations are undergoing gene flow (e.g., during hybridization). Here I experimentally test how assortative mating is maintained with frequent gene flow between diverged head‐color morphs of the Gouldian finch (Erythrura gouldiae). Contrary to the predominant view on the development of sexual preferences in birds, cross‐fostered offspring did not imprint on the phenotype of their conspecific (red or black morphs) or heterospecific (Bengalese finch) foster parents. Instead, the mating preferences of F₁ and F₂ intermorph‐hybrids are consistent with inheritance on the Z chromosomes, which are also the location for genes controlling color expression and the genes causing low fitness of intermorph‐hybrids. Genetic associations between color signal and preference loci on the sex chromosomes may prevent recombination from breaking down these associations when the morphs interbreed, helping to maintain assortative mating in the face of gene flow. Although sex linkage of reproductively isolating traits is theoretically expected to promote speciation, social and ecological constraints may enforce frequent interbreeding between the morphs, thus preventing complete reproductive isolation.     

Hybridization and barriers to gene flow in an island bird radiation

While reinforcement may play a role in all major modes of speciation, relatively little is known about the timescale over which species hybridize without evolving complete reproductive isolation. Birds have high potential for hybridization, and islands provide simple settings for uncovering speciation and hybridization patterns. Here we develop a phylogenetic hypothesis for a phenotypically diverse radiation of finch-like weaver-birds (Foudia) endemic to the western Indian Ocean islands. We find that unlike Darwin's finches, each island-endemic Foudia population is a monophyletic entity for which speciation can be considered complete. In explaining the only exceptions-mismatches between taxonomy, mitochondrial, and nuclear data-phylogenetic and coalescent methods support introgressive hybridization rather than incomplete lineage sorting. Human introductions of known timing of one island-endemic species, to all surrounding archipelagos provide two fortuitous experiments; (1) population sampling at known times in recent evolutionary history, (2) bringing allopatric lineages of an island radiation into secondary contact. Our results put a minimum time bound on introgression (235 years), and support hybridization between species in natural close contact (parapatry), but not between those in natural allopatry brought into contact by human introduction. Time in allopatry, rather than in sympatry, appears key in the reproductive isolation of Foudia species.     

Rapid evolution and the convergence of ecological and evolutionary time

Recent studies have documented rates of evolution of ecologically important phenotypes sufficiently fast that they have the potential to impact the outcome of ecological interactions while they are underway. Observations of this type go against accepted wisdom that ecological and evolutionary dynamics occur at very different time scales. While some authors have evaluated the rapidity of a measured evolutionary rate by comparing it to the overall distribution of measured evolutionary rates, we believe that ecologists are mainly interested in rapid evolution because of its potential to impinge on ecological processes. We therefore propose that rapid evolution be defined as a genetic change occurring rapidly enough to have a measurable impact on simultaneous ecological change. Using this definition we propose a framework for decomposing rates of ecological change into components driven by simultaneous evolutionary change and by change in a non‐evolutionary factor (e.g. density dependent population dynamics, abiotic environmental change). Evolution is judged to be rapid in this ecological context if its contribution to ecological change is large relative to the contribution of other factors. We provide a worked example of this approach based on a theoretical predator–prey interaction [ Abrams, P. & Matsuda, H. (1997) . Evolution, 51, 1740], and find that in this system the impact of prey evolution on predator per capita growth rate is 63% that of internal ecological dynamics. We then propose analytical methods for measuring these contributions in field situations, and apply them to two long‐term data sets for which suitable ecological and evolutionary data exist. For both data sets relatively high rates of evolutionary change have been found when measured as character change in standard deviations per generation (haldanes). For Darwin's finches evolving in response to fluctuating rainfall [ Grant, P.R. & Grant, B.R. (2002) . Science, 296, 707], we estimate that evolutionary change has been more rapid than ecological change by a factor of 2.2. For a population of freshwater copepods whose life history evolves in response to fluctuating fish predation [ Hairston, N.G. Jr & Dillon, T.A. (1990) . Evolution, 44, 1796], we find that evolutionary change has been about one quarter the rate of ecological change – less than in the finch example, but nevertheless substantial. These analyses support the view that in order to understand temporal dynamics in ecological processes it is critical to consider the extent to which the attributes of the system under investigation are simultaneously changing as a result of rapid evolution.     

Sex-specific growth rates in zebra finch nestlings: a possible mechanism for sex ratio adjustment

Wild and captive zebra finches (Taenopygia guttata), like severalother species, produce a male-biased sex ratio at fledging whenfood is scarce. This is due to primary sex-ratio adjustmentand female-biased nestling mortality. Given that young femalesfledging at low body masses have been shown to have low fecundityas adults, lower returns to parents from producing female offspringin conditions of restricted food has been raised as a functionalexplanation (Trivers and Willard's hypothesis of adaptive sexualinvestment; 1973). However, an alternative, mechanistic hypothesisis that under restricted conditions female chicks are more costlyto produce. In consequence, lower returns to parents under theseconditions would happen earlier in the life of female offspringrather than later. To test this hypothesis, I hand-reared chickson a food gradient. In the absence of parent-offspring and sib-sibinteractions, final body mass and growth rates for females werelower in conditions of restricted food. For males, final bodymass and growth rates did not differ with food condition. Lowfemale growth rates in food-restricted conditions might be onepotential mechanism causing female-biased mortality in birds.More importantly, this result is the strongest evidence yetof female offspring experiencing higher marginal fitness benefitsfrom additional food than males and it has implications forprimary and secondary sex-ratio adjustment. Also, as this mechanismhas been shown in the absence of parent-offspring interactions,significant questions can now be raised as to how parental andoffspring behavior interact in their effects on secondary sex-ratioadjustment.     

Simulating secondary contact in allopatric speciation: an empirical test of premating isolation

Allopatric populations of Geospiza difficilis, the Sharp‐beaked Ground Finch, differ morphologically in association with different habitats to an extent unrivalled by any other species of Darwin's finch. The question arises as to whether they have diverged so much that they would not interbreed if they became sympatric; in other words, have they become separate species while remaining allopatric? In other species of Darwin's finches, it is known that a sexual imprinting‐like process based on early learning of song constrains breeding to conspecifics in sympatry. Therefore we used song playback experiments on Isla Genovesa to test the potential of G. difficilis to respond to songs from two other populations of the species on other, ecologically similar, islands. We found strong responses by males to songs of their own population, and heterogeneous but overall weaker responses to the structurally similar songs of G. difficilis from Isla Darwin. Tested birds did not respond to G. difficilis songs from Isla Wolf, songs of G. fuliginosa from Isla Pinta and control Cassin's finch songs. Female responses were infrequent and weak, apparently inhibited by the presence of responding males in most instances. Thus, assuming that females exercise similar discriminations to those of males, the Genovesa population of G. difficilis appears to be well advanced along the path of speciation: reproductively isolated from the Wolf population by a premating barrier to gene exchange that is culturally inherited, but not reproductively isolated from the Darwin population. We discuss the implications of imprinting for the process of speciation, the reasons for divergence of songs in allopatry, and the outcome of a hypothetical secondary contact in terms of coexistence, competition and interbreeding. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 76 , 545–556.