Remarkable new evidence for island radiation in birds

If island biogeography has a sweet spot, it's where islands generate their own species diversity rather than merely taking on mainland immigrants. In birds and other highly dispersive taxa, however, this 'zone of radiation', may be vanishingly small. Darwin's finches and Hawaiian Honeycreepers are among only a handful of examples of island radiation in birds (Price 2008), suggesting that winged powers of dispersal make sufficient isolation from mainland colonists unlikely, while also hindering speciation within and among isolated islands. Nevertheless, two studies in this issue of Molecular Ecology join a string of other recent analyses suggesting that island radiation in birds remains under-appreciated (see also Moyle et al. 2009; Kisel & Barraclough 2010; Rosindell & Phillimore 2011). Melo et al. (2011) use a phylogenetic analysis of white-eyes on islands in the Gulf of Guinea to identify two previously overlooked island radiations, and reveal replicated adaptive divergence on islands where species occur in pairs. Sly et al. (2011), meanwhile, consider possible explanations for speciation and geographic differentiation within a large island, and find the same type of oceanic barriers that are critical to bird speciation across archipelagos may also contribute to divergence that appears to have occurred within a single island.     

Body size evolution in Mesozoic birds: little evidence for Cope's rule

Cope's rule, the tendency towards evolutionary increases in body size, is a long-standing macroevolutionary generalization that has the potential to provide insights into directionality in evolution; however, both the definition and identification of Cope's rule are controversial and problematic. A recent study [J. Evol. Biol. 21 (2008) 618] examined body size evolution in Mesozoic birds, and claimed to have identified evidence of Cope's rule occurring as a result of among-lineage species sorting. We here reassess the results of this study, and additionally carry out novel analyses testing for within-lineage patterns in body size evolution in Mesozoic birds. We demonstrate that the nonphylogenetic methods used by this previous study cannot distinguish between among- and within-lineage processes, and that statistical support for their results and conclusions is extremely weak. Our ancestor-descendant within-lineage analyses explicitly incorporate recent phylogenetic hypotheses and find little compelling evidence for Cope's rule. Cope's rule is not supported in Mesozoic birds by the available data, and body size evolution currently provides no insights into avian survivorship through the Cretaceous-Paleogene mass extinction.     

The patterns and modes of the evolution of disparity in Mesozoic birds

The origin of birds from non-avian theropod dinosaurs is one of the greatest transitions in evolution. Shortly after diverging from other theropods in the Late Jurassic, Mesozoic birds diversified into two major clades—the Enantiornithes and Ornithuromorpha—acquiring many features previously considered unique to the crown group along the way. Here, we present a comparative phylogenetic study of the patterns and modes of Mesozoic bird skeletal morphology and limb proportions. Our results show that the major Mesozoic avian groups are distinctive in discrete character space, but constrained in a morphospace defined by limb proportions. The Enantiornithines, despite being the most speciose group of Mesozoic birds, are much less morphologically disparate than their sister clade, the Ornithuromorpha—the clade that gave rise to living birds, showing disparity and diversity were decoupled in avian history. This relatively low disparity suggests that diversification of enantiornithines was characterized in exhausting fine morphologies, whereas ornithuromorphs continuously explored a broader array of morphologies and ecological opportunities. We suggest this clade-specific evolutionary versatility contributed to their sole survival of the end-Cretaceous mass extinction.     

Historical mutation rates predict susceptibility to radiation in Chernobyl birds

Extreme environmental perturbations are rare, but may have important evolutionary consequences. Responses to current perturbations may provide important information about the ability of living organisms to cope with similar conditions in the evolutionary past. Radioactive contamination from Chernobyl constitutes one such extreme perturbation, with significant but highly variable impact on local population density and mutation rates of different species of animals and plants. We explicitly tested the hypothesis that species with strong impacts of radiation on abundance were those with high rates of historical mutation accumulation as reflected by cytochrome b mitochondrial DNA base‐pair substitution rates during past environmental perturbations. Using a dataset of 32 species of birds, we show higher historical mitochondrial substitution rates in species with the strongest negative impact of local levels of radiation on local population density. These effects were robust to different estimates of impact of radiation on abundance, weighting of estimates of abundance by sample size, statistical control for similarity in the response among species because of common phylogenetic descent, and effects of population size and longevity. Therefore, species that respond strongly to the impact of radiation from Chernobyl are also the species that in the past have been most susceptible to factors that have caused high substitution rates in mitochondrial DNA.     

Evolutionary dynamics of Rh2 opsins in birds demonstrate an episode of accelerated evolution in the New World warblers (Setophaga)

Low rates of sequence evolution associated with purifying selection can be interrupted by episodic changes in selective regimes. Visual pigments are a unique system in which we can investigate the functional consequences of genetic changes, therefore connecting genotype to phenotype in the context of natural and sexual selection pressures. We study the RH2 and RH1 visual pigments (opsins) across 22 bird species belonging to two ecologically convergent clades, the New World warblers (Parulidae) and Old World warblers (Phylloscopidae) and evaluate rates of evolution in these clades along with data from 21 additional species. We demonstrate generally slow evolution of these opsins: both Rh1 and Rh2 are highly conserved across Old World and New World warblers. However, Rh2 underwent a burst of evolution within the New World genus Setophaga, where it accumulated substitutions at 6 amino acid sites across the species we studied. Evolutionary analyses revealed a significant increase in d_N/d_S in Setophaga, implying relatively strong selective pressures to overcome long‐standing purifying selection. We studied the effects of each substitution on spectral tuning and found they do not cause large spectral shifts. Thus, substitutions may reflect other aspects of opsin function, such as those affecting photosensitivity and/or dark–light adaptation. Although it is unclear what these alterations mean for colour perception, we suggest that rapid evolution is linked to sexual selection, given the exceptional plumage colour diversification in Setophaga.     

Phylogenetic eigenvectors and nonstationarity in the evolution of theropod dinosaur skulls

Despite the long‐standing interest in nonstationarity of both phenotypic evolution and diversification rates, only recently have methods been developed to study this property. Here, we propose a methodological expansion of the phylogenetic signal‐representation (PSR) curve based on phylogenetic eigenvectors to test for nonstationarity. The PSR curve is built by plotting the coefficients of determination R² from phylogenetic eigenvector regression (PVR) models increasing the number of phylogenetic eigenvectors against the accumulated eigenvalues. The PSR curve is linear under a stationary model of trait evolution (i.e. the Brownian motion model). Here we describe the distribution of shifts in the models R² and used a randomization procedure to compare observed and simulated shifts along the PSR curve, which allowed detecting nonstationarity in trait evolution. As an applied example, we show that the main evolutionary pattern of variation in the theropod dinosaur skull was nonstationary, with a significant shift in evolutionary rates in derived oviraptorosaurs, an aberrant group of mostly toothless, crested, birdlike theropods. This result is also supported by a recently proposed Bayesian‐based method (AUTEUR). A significant deviation between Ceratosaurus and Limusaurus terminal branches was also detected. We purport that our new approach is a valuable tool for evolutionary biologists, owing to its simplicity, flexibility and comprehensiveness.     

The first 50Myr of dinosaur evolution: macroevolutionary pattern and morphological disparity

The evolutionary radiation of dinosaurs in the Late Triassic and Early Jurassic was a pivotal event in the Earth's history but is poorly understood, as previous studies have focused on vague driving mechanisms and have not untangled different macroevolutionary components (origination, diversity, abundance and disparity). We calculate the morphological disparity (morphospace occupation) of dinosaurs throughout the Late Triassic and Early Jurassic and present new measures of taxonomic diversity. Crurotarsan archosaurs, the primary dinosaur 'competitors', were significantly more disparate than dinosaurs throughout the Triassic, but underwent a devastating extinction at the Triassic-Jurassic boundary. However, dinosaur disparity showed only a slight non-significant increase after this event, arguing against the hypothesis of ecological release-driven morphospace expansion in the Early Jurassic. Instead, the main jump in dinosaur disparity occurred between the Carnian and Norian stages of the Triassic. Conversely, dinosaur diversity shows a steady increase over this time, and measures of diversification and faunal abundance indicate that the Early Jurassic was a key episode in dinosaur evolution. Thus, different aspects of the dinosaur radiation (diversity, disparity and abundance) were decoupled, and the overall macroevolutionary pattern of the first 50Myr of dinosaur evolution is more complex than often considered.     

Mitochondrial genomes of two demosponges provide insights into an early stage of animal evolution

Mitochondrial DNA (mtDNA) of multicellular animals (Metazoa) is typically a small ( approximately 16 kbp), circular-mapping molecule that encodes 37 tightly packed genes. The structures of mtDNA-encoded transfer RNAs (tRNAs) and ribosomal RNAs (rRNAs) are usually highly unorthodox, and proteins are translated with multiple deviations from the standard genetic code. In contrast, mtDNA of the choanoflagellate Monosiga brevicollis, the closest unicellular relative of animals, is four times larger, contains 1.5 times as many genes, and lacks mentioned peculiarities of animal mtDNA. To investigate the evolutionary transition that led to the specific organization of metazoan mtDNA, we determined complete mitochondrial sequences from the demosponges Geodia neptuni and Tethya actinia, two representatives of the most basal animal phylum, the Porifera. We found that poriferan mtDNAs resemble those of other animals in their compact organization, lack of introns, and a well-conserved animal-like gene order. Yet, they contain several extra genes, encode bacterial-like rRNAs and tRNAs, and use a minimally derived genetic code. Our findings suggest that the evolution of the typical metazoan mtDNA has been a multistep process in which the compact genome organization and the reduced gene content were established prior to the reduction of tRNA and rRNA structures and the introduction of multiple changes of the translation code.     

Adaptive molecular evolution of HINTW,a female-specific gene in birds

It is well established that many genes on the male-specific Y chromosome of organisms such as mammals are involved in male reproduction and may evolve rapidly because of positive selection on male reproductive traits. In contrast, very little is known about the function and evolution of W-linked genes restricted to the female genome of organisms with female heterogamety. For birds (males ZZ, females ZW), only one W-linked gene (HINTW) is sufficiently different from its Z-linked homolog to indicate a female-specific function. Here, we report that HINTW shows evidence of adaptive molecular evolution, implying strong positive selection for new functional properties in female birds. Moreover, because HINTW is expressed in the gonads of female birds just before sexual differentiation and is thus a candidate for sex determination, it suggests adaptive evolution related to female development. This provides the first example of Darwinian evolution of a gene restricted to the female genome of any organism. Given that HINTW exists in multiple copies on W, similar to some testis-specific genes amplified on mammalian Y, avian HINTW may thus potentially represent a female parallel to the organization and evolution of Y chromosome genes involved in male reproduction and development.     

Evolution of tooth crown shape in Mesozoic birds,and its adaptive significance with respect to diet

Both the evolution of tooth morphology and the relationship between dental features and diet in toothed birds have long been studied. Here we quantify variation in tooth crown shape in 28 key Mesozoic bird species, and examine differences in dental morphology among birds belonging to different taxonomic groupings and inferred to have had different diets. Using geometric morphometric methods (GMM) and phylogenetic comparative methods (PCM), we found few clear differences in tooth crown shape between different taxonomic and ecological categories, and our analysis provides little support for many dietary inferences drawn in previous studies. However, the Solnhofen Archaeopteryx, Jeholornis, Protopteryx, Pengornis, Longipteryx, Tianyuornis, Mengciusornis, Ichthyornis and Hesperornis all were found to possess relatively specialized tooth crown shapes, perhaps reflecting specialized diets such as insectivory, granivory, piscivory and consumption of soft-shelled arthropods. Similarity in tooth crown shape across many Mesozoic birds may indicate the lack of dietary specialization, and the association between tooth form and diet may have been weakened in any case by ‘functional replacement’ of the dentition by a horny beak and, in many cases, gastroliths.     

Sexual selection accelerates signal evolution during speciation in birds

Sexual selection is proposed to be an important driver of diversification in animal systems, yet previous tests of this hypothesis have produced mixed results and the mechanisms involved remain unclear. Here, we use a novel phylogenetic approach to assess the influence of sexual selection on patterns of evolutionary change during 84 recent speciation events across 23 passerine bird families. We show that elevated levels of sexual selection are associated with more rapid phenotypic divergence between related lineages, and that this effect is restricted to male plumage traits proposed to function in mate choice and species recognition. Conversely, we found no evidence that sexual selection promoted divergence in female plumage traits, or in male traits related to foraging and locomotion. These results provide strong evidence that female choice and male–male competition are dominant mechanisms driving divergence during speciation in birds, potentially linking sexual selection to the accelerated evolution of pre-mating reproductive isolation.     

Disparity vs. diversity in Stegosauria (Dinosauria,Ornithischia): cranial and post-cranial sub-dataset provide different signals

The Stegosauria represents an iconic group of ornithischian dinosaurs, with a fossil record spanning the Middle Jurassic to the Late Cretaceous. In this contribution I present the first detailed analysis of the relationship between disparity and diversity through the evolutionary history of the group. The analysis has been performed on a recently published cladistic dataset, allowing the separate study of the signals deriving from discrete characters and from continuous morphometric characters. Whereas the disparity as sum of variance is decoupled with respect to diversity, the sum of ranges provides a signal fairly consistent with the trend in the number of taxa. Both sub-data sets show that evolution of stegosaurs can be considered essentially as symmetrical, i.e. the maximum exploration of the possible morphospace takes place about half way through the history of the group, with subsequent significant decline until extinction in the Upper Cretaceous. An interesting result is a decoupling of the tempo and mode of evolution of the cranium and postcranium in stegosaurs. Specifically, the evolutionary radiation with maximum saturation of morphospace is anticipated in the cranial skeleton, with maximum peak in the Oxfordian; in contrast, the postcranium explores the largest number of morphotypes subsequently during the Kimmeridgian.     

The evolution of communal roosting in birds: origin and secondary losses

Three main benefits are thought to underlie communal roostingin birds: a reduction in thermoregulation demands, a decreasein predation risk, and an increase in foraging efficiency. Iinvestigated interspecific variation in communal roosting tendenciesacross categories of several ecological factors to examine therelevance of each functional hypothesis in the evolutionary transitionto communal roosting and the secondary reversal to solitary roostinghabits. The study phylogenetic tree included 30 families and437 species. Evolutionary transitions to communal roosting occurredmore often on branches with flocking species and with largerspecies but were not associated with diet, territoriality, geographicalarea, or time of day. The association with flocking activitiessuggests that increased foraging efficiency, a factor thoughtto operate through the formation of flocks, may have been akey factor in the origin of avian communal roosting. However,several transitions to communal roosting occurred on brancheswith nonflocking species, indicating that foraging efficiencymay not be the only factor involved in the evolution of communalroosting. Secondary losses of communal roosting habits occurredon several branches, with a concomitant loss of flocking behaviorand a tendency to exhibit territorial behavior and nocturnalforaging. Secondary losses suggest that communal roosting iscostly to perform and maintain and may be lost when an asocialselection regime operates. The large number of exceptions tothe above patterns may force a reevaluation of current functional hypothesesabout communal roosting in birds.     

Modularity and heterochrony in the evolution of the ceratopsian dinosaur frill

The fossil record provides compelling examples of heterochrony at macroevolutionary scales such as the peramorphic giant antlers of the Irish elk. Heterochrony has also been invoked in the evolution of the distinctive cranial frill of ceratopsian dinosaurs such as Triceratops. Although ceratopsian frills vary in size, shape, and ornamentation, quantitative analyses that would allow for testing hypotheses of heterochrony are lacking. Here, we use geometric morphometrics to examine frill shape variation across ceratopsian diversity and within four species preserving growth series. We then test whether the frill constitutes an evolvable module both across and within species, and compare growth trajectories of taxa with ontogenetic growth series to identify heterochronic processes. Evolution of the ceratopsian frill consisted primarily of progressive expansion of its caudal and caudolateral margins, with morphospace occupation following taxonomic groups. Although taphonomic distortion represents a complicating factor, our data support modularity both across and within species. Peramorphosis played an important role in frill evolution, with acceleration operating early in neoceratopsian evolution followed by progenesis in later diverging cornosaurian ceratopsians. Peramorphic evolution of the ceratopsian frill may have been facilitated by the decoupling of this structure from the jaw musculature, an inference that predicts an expansion of morphospace occupation and higher evolutionary rates among ceratopsids as indeed borne out by our data. However, denser sampling of the meager record of early‐diverging taxa is required to test this further.     

Little evidence for sympatric speciation in island birds

It has been suggested that the presence of sister species in small circumscribed areas, such as isolated lakes or islands, might imply that these species originated sympatrically. To investigate this possibility in birds, we searched for endemic, congeneric species on isolated islands in the ocean. Among 46 islands and small archipelagos chosen because they contain at least one species of endemic land bird, we identified seven pairs of endemic congeners (excluding flightless rails). Of these seven, only four pairs are potentially sister species and thus possible candidates for sympatric speciation. However, three of these four pairs have always been considered the results of double invasion from a mainland source (in two of these cases, molecular-phylogenetic work has either confirmed a double invasion or is ambiguous). The one remaining pair may have speciated allopatrically on a small archipelago. Additional phylogenetic studies are required to understand these cases, and our results should also be considered in light of the large number of island-bird extinctions in historic time. We conclude that, at present, there is little evidence for sympatric speciation in island birds.     

Elevational differentiation accelerates trait evolution but not speciation rates in Amazonian birds

The importance of ecologically mediated divergent selection in accelerating trait evolution has been poorly studied in the most species‐rich biome of the planet, the continental Neotropics. We performed macroevolutionary analyses of trait divergence and diversification rates across closely related pairs of Andean and Amazonian passerine birds, to assess whether the difference in elevational range separating species pairs – a proxy for the degree of ecological divergence – influences the speed of trait evolution and diversification rates. We found that elevational differentiation is associated with faster divergence of song frequency, a trait important for pre‐mating isolation, and several morphological traits, which may contribute to extrinsic post‐mating isolation. However, elevational differentiation did not increase recent speciation rates, possibly due to early bursts of diversification during the uplift of the eastern Andes followed by a slow‐down in speciation rate. Our results suggest that ecological differentiation may speed up trait evolution, but not diversification of Neotropical birds.     

Rapid phenotypic evolution during incipient speciation in a continental avian radiation

Adaptive radiations have helped shape how we view animal speciation, particularly classic examples such as Darwin's finches, Hawaiian fruitflies and African Great Lakes cichlids. These 'island' radiations are comparatively recent, making them particularly interesting because the mechanisms that caused diversification are still in motion. Here, we identify a new case of a recent bird radiation within a continentally distributed species group; the capuchino seedeaters comprise 11 Sporophila species originally described on the basis of differences in plumage colour and pattern in adult males. We use molecular data together with analyses of male plumage and vocalizations to understand species limits of the group. We find marked phenotypic variation despite lack of mitochondrial DNA monophyly and few differences in other putatively neutral nuclear markers. This finding is consistent with the group having undergone a recent radiation beginning in the Pleistocene, leaving genetic signatures of incomplete lineage sorting, introgressive hybridization and demographic expansions. We argue that this apparent uncoupling between neutral DNA homogeneity and phenotypic diversity is expected for a recent group within the framework of coalescent theory. Finally, we discuss how the ecology of open habitats in South America during the Pleistocene could have helped promote this unique and ongoing radiation.     

The evolution of highly variable immunity genes across a passerine bird radiation

To survive, individuals must be able to recognize and eliminate pathogens. The genes of the major histocompatibility complex (MHC) play an essential role in this process in vertebrates as their diversity affects the repertoire of pathogens that can be recognized by the immune system. Emerging evidence suggests that birds within the parvorder Passerida possess an exceptionally high number of MHC genes. However, this has yet to be directly investigated using a consistent framework, and the question of how this MHC diversity has evolved has not been addressed. We used next‐generation sequencing to investigate how MHC class I gene copy number and sequence diversity varies across the Passerida radiation using twelve species chosen to represent the phylogenetic range of this group. Additionally, we performed phylogenetic analyses on this data to identify, for the first time, the evolutionary model that best describes how MHC class I gene diversity has evolved within Passerida. We found evidence of multiple MHC class I genes in every family tested, with an extremely broad range in gene copy number across Passerida. There was a strong phylogenetic signal in MHC gene copy number and diversity, and these traits appear to have evolved through a process of Brownian motion in the species studied, that is following the pattern of genetic drift or fluctuating selection, as opposed to towards a single optimal value or through evolutionary ‘bursts’. By characterizing MHC class I gene diversity across Passerida in a systematic framework, this study provides a first step towards understanding this huge variation.     

Latitudinal gradients in climatic‐niche evolution accelerate trait evolution at high latitudes

Despite the importance of divergent selection to the speed of evolution, it remains poorly understood if divergent selection is more prevalent in the tropics (where species richness is highest), or at high latitudes (where paleoclimate change has been most intense). We tested whether the rate of climatic‐niche evolution – one proxy for divergent selection – varies with latitude for 111 pairs of bird species. Using Brownian motion and Ornsetin–Ulhenbeck models, we show that evolutionary rates along two important axes of the climatic‐niche – temperature and seasonality – have been faster at higher latitudes. We then tested whether divergence of the climatic‐niche was associated with evolution in traits important in ecological differentiation (body mass) and reproductive isolation (song), and found that climatic divergence is associated with faster rates in both measures. These results highlight the importance of climate‐mediated divergent selection pressures in driving evolutionary divergence and reproductive isolation at high latitudes.     

Fossil evidence for key innovations in the evolution of insect diversity

Explaining the taxonomic richness of the insects, comprising over half of all described species, is a major challenge in evolutionary biology. Previously, several evolutionary novelties (key innovations) have been posited to contribute to that richness, including the insect bauplan, wings, wing folding and complete metamorphosis, but evidence over their relative importance and modes of action is sparse and equivocal. Here, a new dataset on the first and last occurrences of fossil hexapod (insects and close relatives) families is used to show that basal families of winged insects (Palaeoptera, e.g. dragonflies) show higher origination and extinction rates in the fossil record than basal wingless groups (Apterygota, e.g. silverfish). Origination and extinction rates were maintained at levels similar to Palaeoptera in the more derived Polyneoptera (e.g. cockroaches) and Paraneoptera (e.g. true bugs), but extinction rates subsequently reduced in the very rich group of insects with complete metamorphosis (Holometabola, e.g. beetles). Holometabola show evidence of a recent slow-down in their high net diversification rate, whereas other winged taxa continue to diversify at constant but low rates. These data suggest that wings and complete metamorphosis have had the most effect on family-level insect macroevolution, and point to specific mechanisms by which they have influenced insect diversity through time.