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Empirical data that identify contemporary mechanisms of divergence shed light on how species could multiply. In this study, we measured population genetic structure, song syllable diversity and response to simulated intruder song in Darwin's small tree finch (Camarhynchus parvulus) on Santa Cruz and Floreana Islands, Galápagos archipelago. Our aim was to test whether the magnitude of contemporary behavioural response in resident birds was consistent with patterns of genetic or cultural differences between populations. We analysed genetic structure and the occurrence of song syllable types, and experimentally measured the response of resident birds to intruder bird song from different geographical origin (i.e., island) or syllable type. We discovered a weak signal of population genetic structure between Santa Cruz and Floreana Islands. Although some song syllables occurred on both islands, others were unique to each island; Santa Cruz Island males used more unique syllables than Floreana Island males. Both Santa Cruz and Floreana resident males discriminated their response towards a simulated intruder song based on the geographical origin of the intruder song, but not on the syllable type sung by the intruder. We conclude that the populations are diverging in genetic and cultural traits and identified a signal of contemporary behavioural response that could maintain divergence upon secondary contact., (© 2021 The Authors. Journal of Evolutionary Biology published by John Wiley & Sons Ltd on behalf of European Society for Evolutionary Biology.)

Birds display advanced behaviors, including vocal learning and problem-solving, yet lack a layered neocortex, a structure associated with complex behavior in mammals. To determine whether these behavioral similarities result from shared or distinct neural circuits, we used single-cell RNA sequencing to characterize the neuronal repertoire of the songbird song motor pathway. Glutamatergic vocal neurons had considerable transcriptional similarity to neocortical projection neurons; however, they displayed regulatory gene expression patterns more closely related to neurons in the ventral pallium. Moreover, while γ-aminobutyric acid-releasing neurons in this pathway appeared homologous to those in mammals and other amniotes, the most abundant avian class is largely absent in the neocortex. These data suggest that songbird vocal circuits and the mammalian neocortex have distinct developmental origins yet contain transcriptionally similar neurons., (Copyright © 2021 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.)

Introgressive hybridization can affect the evolution of populations in several important ways. It may retard or reverse divergence of species, enable the development of novel traits, enhance the potential for future evolution by elevating levels of standing variation, create new species, and alleviate inbreeding depression in small populations. Most of what is known of contemporary hybridization in nature comes from the study of pairs of species, either coexisting in the same habitat or distributed parapatrically and separated by a hybrid zone. More rarely, three species form an interbreeding complex (triad), reported in vertebrates, insects, and plants. Often, one species acts as a genetic link or conduit for the passage of genes (alleles) between two others that rarely, if ever, hybridize. Demographic and genetic consequences are unknown. Here we report results of a long-term study of interbreeding Darwin's finches on Daphne Major island, Galápagos. Geospiza fortis acted as a conduit for the passage of genes between two others that have never been observed to interbreed on Daphne: Geospiza fuliginosa , a rare immigrant, and Geospiza scandens , a resident. Microsatellite gene flow from G. fortis into G. scandens increased in frequency during 30 y of favorable ecological conditions, resulting in genetic and morphological convergence. G. fortis , G. scandens , and the derived dihybrids and trihybrids experienced approximately equal fitness. Especially relevant to young adaptive radiations, where species differ principally in ecology and behavior, these findings illustrate how new combinations of genes created by hybridization among three species can enhance the potential for evolutionary change., Competing Interests: The authors declare no competing interest.

Pyrenestes finches are unique among birds in showing a non-sex-determined polymorphism in bill size and are considered a textbook example of disruptive selection. Morphs breed randomly with respect to bill size, and differ in diet and feeding performance relative to seed hardness. Previous breeding experiments are consistent with the polymorphism being controlled by a single genetic factor. Here, we use genome-wide pooled sequencing to explore the underlying genetic basis of bill morphology and identify a single candidate region. Targeted resequencing reveals extensive linkage disequilibrium across a 300 Kb region containing the insulin-like growth factor 1 (IGF1) gene, with a single 5-million-year-old haplotype associating with phenotypic dominance of the large-billed morph. We find no genetic similarities controlling bill size in the well-studied Darwin's finches (Geospiza). Our results show how a single genetic factor may control bill size and provide a foundation for future studies to examine this phenomenon within and among avian species.

Of the various forms of nonrandom dispersal, matching habitat choice, whereby individuals preferentially reside in habitats where they are best adapted, has relatively little empirical support. Here, I use mark-recapture data to test for matching habitat choice in two nomadic ecotypes of North American Red Crossbills (Loxia curvirostra complex) that exist in the lodgepole pine (Pinus contorta) forests in the South Hills, Idaho, every summer. Crossbills are adapted for foraging on seeds in conifer cones, and in the South Hills the cones are distinctive, favoring a relatively large bill. During a period when seed was most limiting, only the largest individuals approximating the average size of the locally adapted ecotype remained for a year or more. During a period when seed was less limiting, proportionately more individuals remained and the trend for larger individuals to remain was weaker. Although matching habitat choice is difficult to demonstrate, it likely contributed to the observed patterns. Otherwise, nearly unprecedented intensities of natural selection would be needed. Given the nomadic behavior of most crossbill ecotypes and the heterogeneous nature of conifer seed crops, matching habitat choice should be favored and likely contributes to their adaptation to alternative conifers and rapid diversification., (© 2016 The Author(s). Evolution © 2016 The Society for the Study of Evolution.)

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., (© 2016 John Wiley & Sons Ltd.)

We recently used genome sequencing to study the evolutionary history of the Darwin's finches. A prominent feature of our data was that different polymorphic sites in the genome tended to indicate different genetic relationships among these closely related species. Such patterns are expected in recently diverged genomes as a result of incomplete lineage sorting. However, we uncovered conclusive evidence that these patterns have also been influenced by interspecies hybridisation, a process that has likely played an important role in the radiation of Darwin's finches. A major discovery was that segregation of two haplotypes at the ALX1 locus underlies variation in beak shape among the Darwin's finches, and that differences between the two haplotypes in a 240 kb region in blunt and pointed beaked birds involve both coding and regulatory changes. As we review herein, the evolution of such adaptive haplotypes comprising multiple causal changes appears to be an important mechanism contributing to the evolution of biodiversity., (© 2015 WILEY Periodicals, Inc.)

A recent analysis of the genomes of Darwin's finches revealed extensive interspecies allele sharing throughout the history of the radiation and identified a key locus responsible for morphological evolution in this group. The radiation of Darwin's finches on the Galápagos archipelago has long been regarded as an iconic study system for field ecology and evolutionary biology. Coupled with an extensive history of field work, these latest findings affirm the increasing acceptance of introgressive hybridization, or gene flow between species, as a significant contributor to adaptive evolution. Here, we review and discuss these findings in relation to both classical work on Darwin's finches and contemporary work showing similar evolutionary signatures in other biological systems. The continued unification of genomic data with field biology promises to further elucidate the molecular basis of adaptation in Darwin's finches and well beyond., (© 2015 WILEY Periodicals, Inc.)

The trajectory of speciation involves geographic isolation of ancestral populations followed by divergence by natural selection, genetic drift or sexual selection. Once started, the process may experience fits and starts, as sometimes diverging populations intermittently reconnect. In theory populations might cycle between stages of differentiation and never attain species status, a process we refer to as Sisyphean evolution. We argue that the six putative ground finch species (genus Geospiza) of the Galápagos Islands represent a dramatic example of Sisyphean evolution that has been confused with the standard model of speciation. The dynamic environment of the Galápagos, closely spaced islands, and frequent dispersal and introgression have prevented the completion of the speciation process. We suggest that morphological clusters represent locally adapted ecomorphs, which might mimic, and have been confused with, species, but these ecomorphs do not form separate gene pools and are ephemeral in space and time. Thus the pattern of morphological, behavioural and genetic variation supports recognition of a single species of Geospiza, which we suggest should be recognized as Darwin's ground finch (Geospiza magnirostris). We argue that instead of providing an icon of insular speciation and adaptive radiation, which is featured in nearly every textbook on evolutionary biology, Darwin's ground finch represents a potentially more interesting phenomenon, one of transient morphs trapped in an unpredictable cycle of Sisyphean evolution. Instead of revealing details of the origin of species, the mechanisms underlying the transient occurrence of ecomorphs provide one of the best illustrations of the antagonistic effects of natural selection and introgression., (© 2014 The Authors. Biological Reviews © 2014 Cambridge Philosophical Society.)

One of nature's premier illustrations of adaptive evolution concerns the tight correspondence in birds between beak morphology and feeding behavior. In seed-crushing birds, beaks have been suggested to evolve at least in part to avoid fracture. Yet, we know little about mechanical relationships between beak shape, stress dissipation, and fracture avoidance. This study tests these relationships for Darwin's finches, a clade of birds renowned for their diversity in beak form and function. We obtained anatomical data from micro-CT scans and dissections, which in turn informed the construction of finite element models of the bony beak and rhamphotheca. Our models offer two new insights. First, engineering safety factors are found to range between 1 and 2.5 under natural loading conditions, with the lowest safety factors being observed in species with the highest bite forces. Second, size-scaled finite element (FE) models reveal a correspondence between inferred beak loading profiles and observed feeding strategies (e.g. edge-crushing versus tip-biting), with safety factors decreasing for base-crushers biting at the beak tip. Additionally, we identify significant correlations between safety factors, keratin thickness at bite locations, and beak aspect ratio (depth versus length). These lines of evidence together suggest that beak shape indeed evolves to resist feeding forces.

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.

Reasons why chromosomal rearrangements spread to fixation and frequently distinguish related taxa remain poorly understood. We used cytological descriptions of karyotype to identify large pericentric inversions between species of Estrildid finches (family Estrildidae) and a time-dated phylogeny to assess the genomic, geographic, and phylogenetic context of karyotype evolution in this group. Inversions between finch species fixed at an average rate of one every 2.26 My. Inversions were twice as likely to fix on the sex chromosomes compared to the autosomes. A high repeat density on the sex chromosomes may increase mutation rates, but other explanations via mutagenic input are not supported, as the number of inversions on a chromosome does not correlate with its length or map size. Inversions have fixed 3.3× faster in three continental clades than in two island chain clades, and fixation rate correlates with both range size and the number of sympatric species pairs. These results point to adaptation as the dominant mechanism driving fixation and suggest a role for gene flow in karyotype divergence. A review shows that the rapid karyotype evolution observed in the Estrildid finches appears to be more general across birds, and by implication other understudied taxa., (© 2015 The Author(s).)

Many classic examples of adaptive radiations take place within fragmented systems such as islands or mountains, but the roles of mosaic landscapes and variable gene flow in facilitating species diversification is poorly understood. Here we combine phylogenetic and landscape genetic approaches to understand diversification in Darwin's finches, a model adaptive radiation. We combined sequence data from 14 nuclear introns, mitochondrial markers, and microsatellite variation from 51 populations of all 15 recognized species. Phylogenetic species-trees recovered seven major finch clades: ground, tree, vegetarian, Cocos Island, grey and green warbler finches, and a distinct clade of sharp-beaked ground finches (Geospiza cf. difficilis) basal to all ground and tree finches. The ground and tree finch clades lack species-level phylogenetic structure. Interisland gene flow and interspecies introgression vary geographically in predictable ways. First, several species exhibit concordant patterns of population divergence across the channel separating the Galápagos platform islands from the separate volcanic province of northern islands. Second, peripheral islands have more admixed populations while central islands maintain more distinct species boundaries. This landscape perspective highlights a likely role for isolation of peripheral populations in initial divergence, and demonstrates that peripheral populations may maintain genetic diversity through outbreeding during the initial stages of speciation., (© 2014 The Author(s). Evolution © 2014 The Society for the Study of Evolution.)

Quantitative genetic analyses of basal metabolic rate (BMR) can inform us about the evolvability of the trait by providing estimates of heritability, and also of genetic correlations with other traits that may constrain the ability of BMR to respond to selection. Here, we studied a captive population of zebra finches (Taeniopygia guttata) in which selection lines for male courtship rate have been established. We measure BMR in these lines to see whether selection on male sexual activity would change BMR as a potentially correlated trait. We find that the genetic correlation between courtship rate and BMR is practically zero, indicating that the two traits can evolve independently of each other. Interestingly, we find that the heritability of BMR in our population (h(2)=0.45) is markedly higher than was previously reported for a captive zebra finch population from Norway. A comparison of the two studies shows that additive genetic variance in BMR has been largely depleted in the Norwegian population, especially the genetic variance in BMR that is independent of body mass. In our population, the slope of BMR increase with body mass differs not only between the sexes but also between the six selection lines, which we tentatively attribute to genetic drift and/or founder effects being strong in small populations. Our study therefore highlights two things. First, the evolvability of BMR may be less constrained by genetic correlations and lack of independent genetic variation than previously described. Second, genetic drift in small populations can rapidly lead to different evolvabilities across populations.

Theory predicts that sex chromsome linkage should reduce intersexual genetic correlations thereby allowing the evolution of sexual dimorphism. Empirical evidence for sex linkage has come largely from crosses and few studies have examined how sexual dimorphism and sex linkage are related within outbred populations. Here, we use data on an array of different traits measured on over 10,000 individuals from two pedigreed populations of birds (collared flycatcher and zebra finch) to estimate the amount of sex-linked genetic variance (h(2)z ). Of 17 traits examined, eight showed a nonzero h(2)Z estimate but only four were significantly different from zero (wing patch size and tarsus length in collared flycatchers, wing length and beak color in zebra finches). We further tested how sexual dimorphism and the mode of selection operating on the trait relate to the proportion of sex-linked genetic variance. Sexually selected traits did not show higher h(2)Z than morphological traits and there was only a weak positive relationship between h(2)Z and sexual dimorphism. However, given the relative scarcity of empirical studies, it is premature to make conclusions about the role of sex chromosome linkage in the evolution of sexual dimorphism., (© 2012 The Author(s). Evolution© 2012 The Society for the Study of Evolution.)

A previously published phylogeographic analysis of mtDNA sequences from the widespread Palearctic common rosefinch (Carpodacus erythrinus) suggested the existence of three recently diverged groups, corresponding to the Caucasus, central-western Eurasia, and northeastern Eurasia. We re-evaluated the mtDNA data using coalescence methods and added sequence data from a sex-linked gene. The mtDNA gene tree and SAMOVA supported the distinctiveness of the Caucasian group but not the other two groups. However, UPGMA clustering of mtDNA Φ(ST)-values among populations recovered the three groups. The sex-linked gene tree recovered no phylogeographic signal, which was attributed to recent divergence and insufficient time for sorting of alleles. Overall, coalescence methods indicated a lack of gene flow among the three groups, and population expansion in the central-western and northeastern Eurasia groups. These three groups corresponded to named subspecies, further supporting their validity. A species distribution model revealed potential refugia at the Last Glacial Maximum. These three groups, which we hypothesized are in the early stages of speciation, provided an opportunity for testing tenets of ecological speciation. We showed that the early stages of speciation were not accompanied by ecological niche divergence, consistent with other avian studies., (Copyright © 2012 Elsevier Inc. All rights reserved.)

The astonishing variation in the shape and size of bird beaks reflects a wide range of dietary specializations that played an important role in avian diversification. Among Darwin's finches, ground finches (Geospiza spp.) have beaks that represent scaling variations of the same shape, which are generated by alterations in the signaling pathways that regulate growth of the two skeletal components of the beak: the prenasal cartilage (pnc) and the premaxillary bone (pmx). Whether this developmental mechanism is responsible for variation within groups of other closely related bird species, however, has remained unknown. Here, we report that the Caribbean bullfinches (Loxigilla spp.), which are closely related to Darwin's finches, have independently evolved beaks of a novel shape, different from Geospiza, but also varying from each other only in scaling. However, despite sharing the same beak shape, the signaling pathways and tissues patterning Loxigilla beaks differ among the three species. In Loxigilla noctis, as in Geospiza, the pnc develops first, shaped by Bmp4 and CaM signaling, followed by the development of the pmx, regulated by TGFβIIr, β-catenin, and Dkk3 signaling. In contrast, beak morphogenesis in Loxigilla violacea and Loxigilla portoricensis is generated almost exclusively by the pmx through a mechanism in which Ihh and Bmp4 synergize to promote expansion of bone tissue. Together, our results demonstrate high flexibility in the relationship between morphology and underlying developmental causes, where different developmental programs can generate identical shapes, and similar developmental programs can pattern different shapes.

Coevolutionary arms races are a powerful force driving evolution, adaptation, and diversification. They can generate phenotypic polymorphisms that render it harder for a coevolving parasite or predator to exploit any one individual of a given species. In birds, egg polymorphisms should be an effective defense against mimetic brood parasites and are extreme in the African tawny-flanked prinia (Prinia subflava) and its parasite, the cuckoo finch (Anomalospiza imberbis). Here we use models of avian visual perception to analyze the appearance of prinia and cuckoo finch eggs from the same location over 40 years. We show that the two interacting populations have experienced rapid changes in egg traits. Egg colors of both species have diversified over time, expanding into avian color space as expected under negative frequency-dependent selection. Egg pattern showed signatures of both frequency-dependent and directional selection in different traits, which appeared to be evolving independently of one another. Host and parasite appear to be closely tracking one another's evolution, since parasites showed closer color mimicry of contemporaneous hosts. This correlational evidence suggests that hosts and parasites are locked in an ongoing arms race in egg appearance, driven by constant change in the selective advantage of different phenotypes, and that coevolutionary arms races can generate remarkably rapid phenotypic change.

Phylogenetic relationships among the true finches (Fringillidae) have been confounded by the recurrence of similar plumage patterns and use of similar feeding niches. Using a dense taxon sampling and a combination of nuclear and mitochondrial sequences we reconstructed a well resolved and strongly supported phylogenetic hypothesis for this family. We identified three well supported, subfamily level clades: the Holoarctic genus Fringilla (subfamly Fringillinae), the Neotropical Euphonia and Chlorophonia (subfamily Euphoniinae), and the more widespread subfamily Carduelinae for the remaining taxa. Although usually separated in a different family-group taxon (Drepanidinae), the Hawaiian honeycreepers are deeply nested within the Carduelinae and sister to a group of Asian Carpodacus. Other new relationships recovered by this analysis include the placement of the extinct Chaunoproctus ferreorostris as sister to some Asian Carpodacus, a clade combining greenfinches (Carduelis chloris and allies), Rhodospiza and Rhynchostruthus, and a well-supported clade with the aberrant Callacanthis and Pyrrhoplectes together with Carpodacus rubescens. Although part of the large Carduelis-Serinus complex, the poorly known Serinus estherae forms a distinct lineage without close relatives. The traditionally delimited genera Carduelis, Serinus, Carpodacus, Pinicola and Euphonia are polyphyletic or paraphyletic. Based on our results we propose a revised generic classification of finches and describe a new monotypic genus for Carpodacus rubescens., (Copyright © 2011 Elsevier Inc. All rights reserved.)

A phylogenetic tree for the extant Hawaiian honeycreepers charts their diversification over the past 6 million years., (Copyright © 2011 Elsevier Ltd. All rights reserved.)

Mineralocorticoid receptor is the receptor for corticosteroids such as corticosterone or aldosterone. Previously, we found that mineralocorticoid receptor was highly expressed in song nuclei of a songbird, Bengalese finch (Lonchura striata var. domestica). Here, to examine the relationship between mineralocorticoid receptor expression and avian vocal learning, we analyzed mineralocorticoid receptor expression in the developing brain of another vocal learner, budgerigar (Melopsittacus undulatus) and non-vocal learners, quail (Coturnix japonica) and ring dove (Streptopelia capicola). Mineralocorticoid receptor showed vocal control area-related expressions in budgerigars as Bengalese finches, whereas no such mineralocorticoid receptor expressions were seen in the telencephalon of non-vocal learners. Thus, these results suggest the possibility that mineralocorticoid receptor plays a role in vocal development of parrots as songbirds and that the acquisition of mineralocorticoid receptor expression is involved in the evolution of avian vocal learning., (© 2011 The Authors. Development, Growth & Differentiation © 2011 Japanese Society of Developmental Biologists.)

The unparalleled avian diversity of the Neotropics has long been argued to be in large part the evolutionary consequence of the incredible habitat diversity and rugged topography of the Andes mountains. Various scenarios have been proposed to explain how the Andean context could have generated lineage diversification (e.g. vicariant speciation or parapatric speciation across vertical ecological gradients), yet further study on Andean taxa is needed to reveal the relative importance of the different processes. Here we use mitochondrial and nuclear DNA sequences to derive the first phylogenetic hypothesis for Phrygilus (Sierra-Finches), one of the most species-rich genera of mainly Andean passerines. We find strong evidence that the genus is polyphyletic, comprising four distantly related clades with at least nine other genera interspersed between them (Acanthidops, Catamenia, Diglossa, Haplospiza, Idiopsar, Melanodera, Rowettia, Sicalis and Xenodacnis). These four Phrygilus clades coincide with groups previously established mainly on the basis of plumage characters, suggesting single evolutionary origins for each of these. We consider the history of diversification of each clade, analyzing the timing of splitting events, ancestral reconstruction of altitudinal ranges and current geographical distributions. Phrygilus species origins date mainly to the Pleistocene, with representatives diversifying within, out of, and into the Andes. Finally, we explored whether Phrygilus species, especially those with broad altitudinal and latitudinal Andean distributions, showed phylogeographic structure. Our best-sampled taxon (Phrygilus fruticeti) exhibited no clear pattern; however, we found deep genetic splits within other surveyed species, with Phrygilus unicolor being the most extreme case and deserving of further research., (Copyright © 2011 Elsevier Inc. All rights reserved.)

Despite decades of research, whether vertebrates can and do adaptively adjust the sex ratio of their offspring is still highly debated. However, this may have resulted from the failure of empirical tests to identify large and predictable fitness returns to females from strategic adjustment. Here, we test the effect of diet quality and maternal condition on facultative sex ratio adjustment in the color polymorphic Gouldian finch (Erythrura gouldiae), a species that exhibits extreme maternal allocation in response to severe and predictable (genetically-determined) fitness costs. On high-quality diets, females produced a relatively equal sex ratio, but over-produced sons in poor dietary conditions. Despite the lack of sexual size dimorphism, nutritionally stressed foster sons were healthier, grew faster, and were more likely to survive than daughters. Although these findings are in line with predictions from sex allocation theory, the extent of adjustment is considerably lower than previously reported for this species. Females therefore have strong facultative control over sex allocation, but the extent of adjustment is likely determined by the relative magnitude of fitness gains and the ability to reliably predict sex-specific benefits from environmental (vs. genetic) variables. These findings may help explain the often inconsistent, weak, or inconclusive empirical evidence for adaptive sex ratio adjustment in vertebrates., (© 2011 The Author(s). Evolution© 2011 The Society for the Study of Evolution.)

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., (© 2011 The Author(s). Evolution© 2011 The Society for the Study of Evolution.)

Bird beaks display tremendous variation in shape and size, which is closely associated with the exploitation of multiple ecological niches and likely played a key role in the diversification of thousands of avian species. Previous studies have demonstrated some of the molecular mechanisms that regulate morphogenesis of the prenasal cartilage, which forms the initial beak skeleton. However, much of the beak diversity in birds depends on variation in the premaxillary bone. It forms later in development and becomes the most prominent functional and structural component of the adult upper beak/jaw, yet its regulation is unknown. Here, we studied a group of Darwin's finch species with different beak shapes. We found that TGFβIIr, β-catenin, and Dickkopf-3, the top candidate genes from a cDNA microarray screen, are differentially expressed in the developing premaxillary bone of embryos of species with different beak shapes. Furthermore, our functional experiments demonstrate that these molecules form a regulatory network governing the morphology of the premaxillary bone, which differs from the network controlling the prenasal cartilage, but has the same species-specific domains of expression. These results offer potential mechanisms that may explain how the tightly coupled depth and width dimensions can evolve independently. The two-module program of development involving independent regulating molecules offers unique insights into how different developmental pathways may be modified and combined to induce multidimensional shifts in beak morphology. Similar modularity in development may characterize complex traits in other organisms to a greater extent than is currently appreciated.

Most of our knowledge of sex-chromosome evolution comes from male heterogametic (XX/XY) taxa. With the genome sequencing of multiple female heterogametic (ZZ/ZW) taxa, we can now ask whether there are patterns of evolution common to both sex chromosome systems. In all XX/XY systems examined to date, there is an excess of testis-biased retrogenes moving from the X chromosome to the autosomes, which is hypothesized to result from either sexually antagonistic selection or escape from meiotic sex chromosome inactivation (MSCI). We examined RNA-mediated (retrotransposed) and DNA-mediated gene movement in two independently evolved ZZ/ZW systems, birds (chicken and zebra finch) and lepidopterans (silkworm). Even with sexually antagonistic selection likely operating in both taxa and MSCI having been identified in the chicken, we find no evidence for an excess of genes moving from the Z chromosome to the autosomes in either lineage. We detected no excess for either RNA- or DNA-mediated duplicates, across a range of approaches and methods. We offer some potential explanations for this difference between XX/XY and ZZ/ZW sex chromosome systems, but further work is needed to distinguish among these hypotheses. Regardless of the root causes, we have identified an additional, potentially inherent, difference between XX/XY and ZZ/ZW systems.

The link between adaptation and evolutionary change remains the most central and least understood evolutionary problem. Rapid evolution and diversification of avian beaks is a textbook example of such a link, yet the mechanisms that enable beak's precise adaptation and extensive adaptability are poorly understood. Often observed rapid evolutionary change in beaks is particularly puzzling in light of the neo-Darwinian model that necessitates coordinated changes in developmentally distinct precursors and correspondence between functional and genetic modularity, which should preclude evolutionary diversification. I show that during first 19 generations after colonization of a novel environment, house finches (Carpodacus mexicanus) express an array of distinct, but adaptively equivalent beak morphologies-a result of compensatory developmental interactions between beak length and width in accommodating microevolutionary change in beak depth. Directional selection was largely confined to the elimination of extremes formed by these developmental interactions, while long-term stabilizing selection along a single axis-beak depth-was mirrored in the structure of beak's additive genetic covariance. These results emphasize three principal points. First, additive genetic covariance structure may represent a historical record of the most recurrent developmental and functional interactions. Second, adaptive equivalence of beak configurations shields genetic and developmental variation in individual components from depletion by natural selection. Third, compensatory developmental interactions among beak components can generate rapid reorganization of beak morphology under novel conditions and thus greatly facilitate both the evolution of precise adaptation and extensive diversification, thereby linking adaptation and adaptability in this classic example of Darwinian evolution.

Background: Females often express the same ornaments as males to a similar or lesser degree. Female ornaments can be adaptive, but little is known regarding their origins and mode of evolution. Current utility does not imply evolutionary causation, and therefore it is possible that female ornamentation evolved due to selection on females, as a correlated response to selection on males (sexual constraint), or a combination of both. We tested these ideas simulating simple models for the evolution of male and female correlated traits, and compared their predictions against the coloration of finches in the genus Carduelis., Results: For carotenoid-based ornamental coloration, a model of sexual constraint on females fits the Carduelis data well. The two alternative models (sexual constraint on males, and mutual constraint) were rejected as causing the similarities in carotenoid coloration between males and females. For melanin coloration, the correlation between the sexes was weaker, indicating that males and females evolved independently to a greater extent., Conclusions: This indicates that sexual constraint on females was an important mechanism for the evolution of ornamental carotenoid coloration in females, but less so for melanin coloration. This does not mean that female carotenoid coloration is non-adaptive or maladaptive, because sexual dichromatism could evolve if it were maladaptive. It suggests, however, that most evolution of female carotenoid coloration was male-driven and, when adaptive, may not be an adaptation stricto sensu.

The traditional view is that evolution proceeds very slowly, over immense periods of time, driven by weak selection acting on innumerable genes of small effect. Recent studies of rapid evolution, in the laboratory and in the field, have given a radically different picture. Although beneficial mutations tend to be small in effect when they first appear, those that survive to spread and become fixed are usually among the minority with large effect. Hence, although hundreds of loci of small effect may contribute to variation in character state, adaptation is predominantly caused by alleles of large effect. This leads to the hope that the particular mutations responsible for adaptation to altered conditions of life can be identified and characterized. This has been achieved in some cases and may soon become routine. Furthermore, it raises the possibility that adaptive change can be predicted from a knowledge of genetics and ecology. Experimental evolution suggests that any given selection line that is adapting to changed conditions will follow one of a few themes (broadly speaking, loci), each of which may have many variations (mutations within the locus producing similar phenotypes). Hence, evolutionary change can be predicted only within limits, even in principle. Nevertheless, recent attempts to predict how very simple genomes change have been surprisingly successful, and we may be close to a new predictive understanding of the genetic basis of adaptation.

Divergent selection on traits involved in both local adaptation and the production of mating signals can strongly facilitate population differentiation. Because of its links to foraging morphologies and cultural inheritance song of birds can contribute particularly strongly to maintenance of local adaptations. In two adjacent habitats--native Sonoran desert and urban areas--house finches (Carpodacus mexicanus) forage on seeds that are highly distinct in size and shell hardness and require different bite forces and bill morphologies. Here, we first document strong and habitat-specific natural selection on bill traits linked to bite force and find adaptive modifications of bite force and bill morphology and associated divergence in courtship song between the two habitats. Second, we investigate the developmental basis of this divergence and find that early ontogenetic tissue transformation in bill, but not skeletal traits, is accelerated in the urban population and that the mandibular primordia of the large-beaked urban finches express bone morphogenetic proteins (BMP) earlier and at higher level than those of the desert finches. Further, we show that despite being geographically adjacent, urban and desert populations are nevertheless genetically distinct corroborating findings of early developmental divergence between them. Taken together, these results suggest that divergent selection on function and development of traits involved in production of mating signals, in combination with localized learning of such signals, can be very effective at maintaining local adaptations, even at small spatial scales and in highly mobile animals.

Background: The origin of complex adaptations is one of the most controversial questions in biology. Environmental induction of novel phenotypes, where phenotypic retention of adaptive developmental variation is enabled by organismal complexity and homeostasis, can be a starting point in the evolution of some adaptations, but empirical examples are rare. Comparisons of populations that differ in historical recurrence of environmental induction can offer insight into its evolutionary significance, and recent colonization of North America by the house finch (Carpodacus mexicanus) provides such an opportunity., Results: In both native (southern Arizona) and newly established (northern Montana, 18 generations) populations, breeding female finches exhibit the same complex adaptation - a sex-bias in ovulation sequence - in response to population-specific environmental stimulus of differing recurrence. We document that, in the new population, the adaptation is induced by a novel environment during females' first breeding and is subsequently retained across breeding attempts. In the native population, first-breeding females expressed a precise adaptive response to a recurrent environmental stimulus without environmental induction. We document strong selection on environmental cue recognition in both populations and find that rearrangement of the same proximate mechanism - clustering of oocytes that become males and females - can enable an adaptive response to distinct environmental stimuli., Conclusion: The results show that developmental plasticity induced by novel environmental conditions confers significant fitness advantages to both maternal and offspring generations and might play an important role not only in the successful establishment of this invasive species across the widest ecological range of extant birds, but also can link environmental induction and genetic inheritance in the evolution of novel adaptations.

We present molecular data documenting how introduction to the eastern United States and an epizootic involving a bacterial pathogen has affected the genetic diversity of house finches, a cardueline songbird. Population bottlenecks during introduction can cause loss of genetic variation and may negatively affect a population's ability to adapt to novel stressors such as disease. Although a genome-wide survey using Amplified Fragment Length Polymorphism (AFLP) markers suggests little loss of genetic diversity in introduced populations, an epizootic of bacterial Mycoplasma has nonetheless caused dramatic declines in the eastern US population. Sequence analysis of a candidate gene for pathogen resistance in the Major Histocompatibity Complex (MHC) in pre- and post-epizootic population samples reveals allele frequency shifts since introduction of the pathogen, but similar shifts are also observed in control populations not exposed to the bacteria, and in a neutral non-coding locus. Expression studies using a novel subtractive hybridization approach indicate decreased expression of the class II MHC locus upon exposure to Mycoplasma, a pattern also seen in MHC class I loci in mice infected with cytomegalovirus and consistent with manipulation of the finch immune system by Mycoplasma. These results will be further expanded using experimental studies as well as examination of evolution of the pathogen genome itself.

A classic textbook example of adaptive radiation under natural selection is the evolution of 14 closely related species of Darwin's finches (Fringillidae, Passeriformes), whose primary diversity lies in the size and shape of their beaks. Thus, ground finches have deep and wide beaks, cactus finches have long and pointed beaks (low depth and narrower width), and warbler finches have slender and pointed beaks, reflecting differences in their respective diets. Previous work has shown that even small differences in any of the three major dimensions (depth, width and length) of the beak have major consequences for the overall fitness of the birds. Recently we used a candidate gene approach to explain one pathway involved in Darwin's finch beak morphogenesis. However, this type of analysis is limited to molecules with a known association with craniofacial and/or skeletogenic development. Here we use a less constrained, complementary DNA microarray analysis of the transcripts expressed in the beak primordia to find previously unknown genes and pathways whose expression correlates with specific beak morphologies. We show that calmodulin (CaM), a molecule involved in mediating Ca2+ signalling, is expressed at higher levels in the long and pointed beaks of cactus finches than in more robust beak types of other species. We validated this observation with in situ hybridizations. When this upregulation of the CaM-dependent pathway is artificially replicated in the chick frontonasal prominence, it causes an elongation of the upper beak, recapitulating the beak morphology of the cactus finches. Our results indicate that local upregulation of the CaM-dependent pathway is likely to have been a component of the evolution of Darwin's finch species with elongated beak morphology and provide a mechanistic explanation for the independence of beak evolution along different axes. More generally, our results implicate the CaM-dependent pathway in the developmental regulation of craniofacial skeletal structures.

Maternal modification of offspring sex in birds has strong fitness consequences, however the mechanisms by which female birds can bias sex of their progeny in close concordance with the environment of breeding are not known. In recently established populations of house finches (Carpodacus mexicanus), breeding females lay a sex-biased sequence of eggs when ambient temperature causes early onset of incubation. We studied the mechanisms behind close association of incubation and sex-determination strategies in this species and discovered that pre-ovulation oocytes that produce males and females differed strongly in the temporal patterns of proliferation and growth. In turn, sex-specific exposure of oocytes to maternal secretion of prolactin and androgens produced distinct accumulation of maternal steroids in oocyte yolks in relation to oocyte proliferation order. These findings suggest that sex difference in oocyte growth and egg-laying sequence is an adaptive outcome of hormonal constraints imposed by the overlap of early incubation and oogenesis in this population, and that the close integration of maternal incubation, oocytes' sex-determination and growth might be under control of the same hormonal mechanism. We further document that population establishment and the evolution of these maternal strategies is facilitated by their strong effects on female and offspring fitness in a recently established part of the species range.

Adaptive evolution is often strongly influenced by maternal inheritance that transfers the parental strategies across generations. The consequences of maternal effects for the offspring generation depend on the between-generation similarity in environments and on the evolved sensitivity of the offspring's ontogeny to maternal effects. When these factors differ between sons and daughters, maternal effects can influence the evolution of sexual dimorphism. The establishment of house finch populations across western Montana during the last 30 years was accompanied by rapid evolutionary change in sexual size dimorphism. Here I show that traits that changed the most across generations were most influenced by maternal effects in males but not females. Maternal effects differentially affected sons' and daughters' survival; greater maternal effects were commonly associated with higher survival of sons, especially when maternal and offspring environments were similar. Stronger maternal effects extended preselection phenotypic variance in morphological traits of males, thereby producing some locally adaptive phenotypes and lessening juvenile mortality. Thus, the observed sex-specific maternal effects and their contribution to the evolution of sexual size dimorphism are likely a passive consequence of the distinct sensitivity of sons and daughters to maternal adaptations to breeding in ecologically distinct parts of the house finch's expanding range.

The question we address in this article is how hybridization in the recent past can be detected in recently evolved species. Such species may not have evolved genetic incompatibilities and may hybridize with little or no fitness loss. Hybridization can be recognized by relatively small genetic differences between sympatric populations because sympatric populations have the opportunity to interbreed whereas allopatric populations do not. Using microsatellite DNA data from Darwin's finches in the Galapagos archipelago, we compare sympatric and allopatric genetic distances in pairs of Geospiza and Camarhynchus species. In agreement with the hybridization hypothesis, we found a statistically strong tendency for a species to be more similar genetically to a sympatric relative than to allopatric populations of that relative. Hybridization has been studied directly on two islands, but it is evidently more widespread in the archipelago. We argue that introgressive hybridization may have been a persistent feature of the adaptive radiation through most of its history, facilitating evolutionary diversification and occasionally affecting both the speed and direction of evolution.