Complementarity in Allen's and Bergmann's rules among birds.

Biologists have long noted that endotherms tend to have larger bodies (Bergmann's rule) and shorter appendages (Allen's rule) in colder environments. Nevertheless, many taxonomic groups appear not to conform to these 'rules', and general explanations for these frequent exceptions are currently lacking. Here we note that by combining complementary changes in body and extremity size, lineages could theoretically respond to thermal gradients with smaller changes in either trait than those predicted by either Bergmann's or Allen's rule alone. To test this idea, we leverage geographic, ecological, phylogenetic, and morphological data on 6,974 non-migratory terrestrial bird species, and show that stronger family-wide changes in bill size over thermal gradients are correlated with more muted changes in body size. Additionally, we show that most bird families exhibit weak but appropriately directed changes in both traits, supporting the notion of complementarity in Bergmann's and Allen's rules. Finally, we show that the few families that exhibit significant gradients in either bill or body size, tend to be more speciose, widely distributed, or ecologically constrained. Our findings validate Bergmann's and Allen's logic and remind us that body and bill size are simply convenient proxies for their true quantity of interest: the surface-to-volume ratio.

Neuron numbers link innovativeness with both absolute and relative brain size in birds.

A longstanding issue in biology is whether the intelligence of animals can be predicted by absolute or relative brain size. However, progress has been hampered by an insufficient understanding of how neuron numbers shape internal brain organization and cognitive performance. On the basis of estimations of neuron numbers for 111 bird species, we show here that the number of neurons in the pallial telencephalon is positively associated with a major expression of intelligence: innovation propensity. The number of pallial neurons, in turn, is greater in brains that are larger in both absolute and relative terms and positively covaries with longer post-hatching development periods. Thus, our analyses show that neuron numbers link cognitive performance to both absolute and relative brain size through developmental adjustments. These findings help unify neuro-anatomical measures at multiple levels, reconciling contradictory views over the biological significance of brain expansion. The results also highlight the value of a life history perspective to advance our understanding of the evolutionary bases of the connections between brain and cognition.

Phylogeography and Prevalence of Hemoparasites (Apicomplexa: Eucoccidiorida) in Galápagos Marine Iguanas, Amblyrhynchus cristatus (Reptilia: Iguanidae).

Parasitism is among the most common forms of coexistence of organisms of different species. Hemoparasites live in the bloodstream of the host where they complete different life-cycle stages. Members of the phylum Apicomplexa constitute a large portion of all hemoparasites infecting reptiles and their parasite transmitting vectors, including arthropods. In this study, we carried out a survey and molecular identification of hemoparasites in blood samples of the iconic Galápagos marine iguana (Amblyrhynchus cristatus). Major island populations of marine iguanas were sampled to examine large-scale biogeographic patterns of parasite diversity and prevalence. Nested PCRs were used to amplify segments of the 18S rRNA-gene of hemoparasites. Furthermore, ticks attached to marine iguanas were collected and analyzed in the same way to assess their potential use as a non-invasive method for the detection of hemoparasites in vertebrate host species. PCR products were sequenced and a phylogenetic analysis was carried out showing the presence of two genetically distinct clusters of hemoparasites, one more commonly distributed than the other one, belonging to the genera Hepatozoon and/or Hemolivia (Apicomplexa: Eucoccidiorida). Overall, 25% of marine iguanas were infected by hemoparasites. However, infection rates varied strongly among particular island populations (from 3.45% to 50%). Although marine iguanas are an extremely mobile species that has colonized all islands in the Galápagos archipelago, parasite occurrence was not related to geographical distance, suggesting that dispersal behavior has a minor role in parasite transmission. On most islands, females tended to have higher infection rates than males, but this relationship was only significant on one island. Overall, ticks and marine iguanas had similar prevalence and diversity of parasites. However, the infection profiles of ticks and their corresponding hosts (marine iguanas) did not mirror one another, indicating that this method cannot be used reliably to assess marine iguana infection status. Interestingly, we found that hemoparasite prevalence in marine iguanas and ticks tended to be positively correlated across islands. Our results indicate that certain populations of marine iguanas may have special mechanisms and adaptations to cope with parasite infection. In addition, other factors such as vector density, anthropogenic-related activities or the immunological state of marine iguanas could potentially affect the striking variation in hemoparasite prevalence across island populations.

Niche expansion and adaptive divergence in the global radiation of crows and ravens.

The processes that allow some lineages to diversify rapidly at a global scale remain poorly understood. Although earlier studies emphasized the importance of dispersal, global expansions expose populations to novel environments and may also require adaptation and diversification across new niches. In this study, we investigated the contributions of these processes to the global radiation of crows and ravens (genus Corvus). Combining a new phylogeny with comprehensive phenotypic and climatic data, we show that Corvus experienced a massive expansion of the climatic niche that was coupled with a substantial increase in the rates of species and phenotypic diversification. The initiation of these processes coincided with the evolution of traits that promoted dispersal and niche expansion. Our findings suggest that rapid global radiations may be better understood as processes in which high dispersal abilities synergise with traits that, like cognition, facilitate persistence in new environments.

A test of Darwin's naturalization conundrum in birds reveals enhanced invasion success in the presence of close relatives.

Biological invasions pose one of the most severe environmental challenges of the twenty-first century. A longstanding idea is that invasion risk is predictable based on the phylogenetic distance - and hence ecological resemblance - between non-native and native species. However, current evidence is contradictory. To explain these mixed results, it has been proposed that the effect is scale-dependent, with invasion inhibited by phylogenetic similarity at small spatial scales but enhanced at larger scales. Analyzing invasion outcomes in a global sample of bird communities, we find no evidence to support this hypothesis. Instead, our results suggest that invaders are locally more successful in the presence of closely related and ecologically similar species, at least in human-altered environments where the majority of invasions have occurred. Functional trait analyses further confirm that the ecological niches of invaders are phylogenetically conserved, supporting the notion that successful invasion in the presence of close relatives is driven by shared adaptations to the types of niches available in novel environments.

Phenotypic responses to climate change are significantly dampened in big-brained birds.

Anthropogenic climate change is rapidly altering local environments and threatening biodiversity throughout the world. Although many wildlife responses to this phenomenon appear largely idiosyncratic, a wealth of basic research on this topic is enabling the identification of general patterns across taxa. Here, we expand those efforts by investigating how avian responses to climate change are affected by the ability to cope with ecological variation through behavioural flexibility (as measured by relative brain size). After accounting for the effects of phylogenetic uncertainty and interspecific variation in adaptive potential, we confirm that although climate warming is generally correlated with major body size reductions in North American migrants, these responses are significantly weaker in species with larger relative brain sizes. Our findings suggest that cognition can play an important role in organismal responses to global change by actively buffering individuals from the environmental effects of warming temperatures.

Functional genomics of abiotic environmental adaptation in lacertid lizards and other vertebrates.

Understanding the genomic basis of adaptation to different abiotic environments is important in the context of climate change and resulting short-term environmental fluctuations. Using functional and comparative genomics approaches, we here investigated whether signatures of genomic adaptation to a set of environmental parameters are concentrated in specific subsets of genes and functions in lacertid lizards and other vertebrates. We first identify 200 genes with signatures of positive diversifying selection from transcriptomes of 24 species of lacertid lizards and demonstrate their involvement in physiological and morphological adaptations to climate. To understand how functionally similar these genes are to previously predicted candidate functions for climate adaptation and to compare them with other vertebrate species, we then performed a meta-analysis of 1,100 genes under selection obtained from -omics studies in vertebrate species adapted to different abiotic factors. We found that the vertebrate gene set formed a tightly connected interactome, which was to 23% enriched in previously predicted functions of adaptation to climate, and to a large part (18%) involved in organismal stress response. We found a much higher degree of identical genes being repeatedly selected among different animal groups (43.6%), and of functional similarity and post-translational modifications than expected by chance, and no clear functional division between genes used for ectotherm and endotherm physiological strategies. In total, 171 out of 200 genes of Lacertidae were part of this network. These results highlight an important role of a comparatively small set of genes and their functions in environmental adaptation and narrow the set of candidate pathways and markers to be used in future research on adaptation and stress response related to climate change.

Niche shifts after island colonization spurred adaptive diversification and speciation in a cosmopolitan bird clade.

Islands have long been recognized as key contributors to biodiversity because they facilitate geographic isolation and ecological divergence from mainland ancestors. However, island colonization has traditionally been considered an evolutionary dead-end process, and its consequences for continental biodiversity remain understudied. Here, we use the evolutionary radiation of Columbiformes (i.e. pigeons and doves) to examine if ecological niche shifts on islands shaped biological diversification and community composition on continents. We show that the colonization of islands by continental, terrestrial-foraging lineages led to the exploitation of a new ecological niche (i.e. arboreal foraging). This transition towards arboreal foraging was associated with evolutionary adaptation towards a new morphological optimum. In addition, arboreal-foraging lineages of islands experienced an increase in speciation rates, which was associated with successful range expansions to other islands as well as back colonization of continents. Our results provide empirical evidence that diversification on continents can only be fully understood when studying the diversification processes that took place on islands, challenging the view of islands as mere sinks of evolutionary diversity.

Bryophyte C:N:P stoichiometry, biogeochemical niches and elementome plasticity driven by environment and coexistence.

Ecological stoichiometry and studies of biogeochemical niches have mainly focused on plankton and vascular plants, but the phenotypically closest modern relatives of early plants, bryophytes, have been largely neglected. We analysed C:N:P stoichiometries and elemental compositions (K, Na, Mg, Ca, S, Fe) of 35 widely distributed bryophyte species inhabiting springs. We estimated bryophyte C:N:P ratios and their biogeochemical niches, investigated how elementomes respond to the environment and determined whether they tend to diverge more for coexisting than non-coexisting individuals and species. The median C:N:P was 145:8:1, intermediate between Redfield's ratio for marine plankton and those for vascular plants. Biogeochemical niches were differentiated amongst species and were phylogenetically conserved. Differences in individual and species-specific elementomes increased with coexistence between species. Our results provide an evolutionary bridge between the ecological stoichiometries of algae and vascular plants and suggest that differences in elementomes could be used to understand community assemblages and functional diversity.

Feeding specialization and longer generation time are associated with relatively larger brains in bees.

Despite their miniature brains, insects exhibit substantial variation in brain size. Although the functional significance of this variation is increasingly recognized, research on whether differences in insect brain sizes are mainly the result of constraints or selective pressures has hardly been performed. Here, we address this gap by combining prospective and retrospective phylogenetic-based analyses of brain size for a major insect group, bees (superfamily Apoidea). Using a brain dataset of 93 species from North America and Europe, we found that body size was the single best predictor of brain size in bees. However, the analyses also revealed that substantial variation in brain size remained even when adjusting for body size. We consequently asked whether such variation in relative brain size might be explained by adaptive hypotheses. We found that ecologically specialized species with single generations have larger brains-relative to their body size-than generalist or multi-generation species, but we did not find an effect of sociality on relative brain size. Phylogenetic reconstruction further supported the existence of different adaptive optima for relative brain size in lineages differing in feeding specialization and reproductive strategy. Our findings shed new light on the evolution of the insect brain, highlighting the importance of ecological pressures over social factors and suggesting that these pressures are different from those previously found to influence brain evolution in other taxa.

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.

Gliding Dragons and Flying Squirrels: Diversifying versus Stabilizing Selection on Morphology following the Evolution of an Innovation.

Evolutionary innovations and ecological competition are factors often cited as drivers of adaptive diversification. Yet many innovations result in stabilizing rather than diversifying selection on morphology, and morphological disparity among coexisting species can reflect competitive exclusion (species sorting) rather than sympatric adaptive divergence (character displacement). We studied the innovation of gliding in dragons (Agamidae) and squirrels (Sciuridae) and its effect on subsequent body size diversification. We found that gliding either had no impact (squirrels) or resulted in strong stabilizing selection on body size (dragons). Despite this constraining effect in dragons, sympatric gliders exhibit greater size disparity compared with allopatric gliders, a pattern consistent with, although not exclusively explained by, ecological competition changing the adaptive landscape of body size evolution to induce character displacement. These results show that innovations do not necessarily instigate further differentiation among species, as is so often assumed, and suggest that competition can be a powerful force generating morphological divergence among coexisting species, even in the face of strong stabilizing selection.

Environmental temperatures shape thermal physiology as well as diversification and genome-wide substitution rates in lizards.

Climatic conditions changing over time and space shape the evolution of organisms at multiple levels, including temperate lizards in the family Lacertidae. Here we reconstruct a dated phylogenetic tree of 262 lacertid species based on a supermatrix relying on novel phylogenomic datasets and fossil calibrations. Diversification of lacertids was accompanied by an increasing disparity among occupied bioclimatic niches, especially in the last 10 Ma, during a period of progressive global cooling. Temperate species also underwent a genome-wide slowdown in molecular substitution rates compared to tropical and desert-adapted lacertids. Evaporative water loss and preferred temperature are correlated with bioclimatic parameters, indicating physiological adaptations to climate. Tropical, but also some populations of cool-adapted species experience maximum temperatures close to their preferred temperatures. We hypothesize these species-specific physiological preferences may constitute a handicap to prevail under rapid global warming, and contribute to explaining local lizard extinctions in cool and humid climates.

An integrative study of island diversification: Insights from the endemic Haemodracon geckos of the Socotra Archipelago.

The Socotra Archipelago in the Arabian Sea is considered one of the most geo-politically isolated landforms on earth and a center of endemism. The archipelago is located at the western edge of the Indian Ocean and comprises four islands: Socotra, Darsa, Samha, and Abd al Kuri. Here we provide an integrative study on Haemodracon geckos, the sole genus of geckos strictly endemic to the archipelago. The sympatric distribution of Haemodracon riebeckii and H. trachyrhinus on Socotra Island provides a unique opportunity to explore evolutionary relationships and speciation patterns, examining the interplay between possible sympatric and allopatric scenarios. We used molecular data for phylogenetic inference, species delimitation analyses, and to infer the diversification timeframe. Multivariate statistics were used to analyze morphological data. Ecological comparisons were explored for macro-niches using species distribution models and observations were used for micro-habitat use. Haemodracon species exhibit great levels of intraspecific genetic diversity. Our calibration estimates revealed that Haemodracon diverged from its closest relative, the mainland genus Asaccus, in the Eocene, before the detachment of the archipelago. The two Haemodracon species diversified in situ on Socotra Island during the Middle Miocene, after the archipelago's isolation, into the two reciprocally monophyletic recognized species. Their divergence is associated mostly with remarkable body size differences and micro-habitat segregation, with low levels of climatic and body shape divergences within their sympatric distributions. These results display how ecological, sympatric speciation, and allopatric speciation followed by secondary contact, may both have varying roles at different evolutionary phases.

Oldest skeleton of a fossil flying squirrel casts new light on the phylogeny of the group.

Flying squirrels are the only group of gliding mammals with a remarkable diversity and wide geographical range. However, their evolutionary story is not well known. Thus far, identification of extinct flying squirrels has been exclusively based on dental features, which, contrary to certain postcranial characters, are not unique to them. Therefore, fossils attributed to this clade may indeed belong to other squirrel groups. Here we report the oldest fossil skeleton of a flying squirrel (11.6 Ma) that displays the gliding-related diagnostic features shared by extant forms and allows for a recalibration of the divergence time between tree and flying squirrels. Our phylogenetic analyses combining morphological and molecular data generally support older dates than previous molecular estimates (~23 Ma), being congruent with the inclusion of some of the earliest fossils (~36 Ma) into this clade. They also show that flying squirrels experienced little morphological change for almost 12 million years.

Diversity, distribution and conservation of the terrestrial reptiles of Oman (Sauropsida, Squamata).

In the present work, we use an exceptional database including 5,359 records of 101 species of Oman's terrestrial reptiles together with spatial tools to infer the spatial patterns of species richness and endemicity, to infer the habitat preference of each species and to better define conservation priorities, with especial focus on the effectiveness of the protected areas in preserving this unique arid fauna. Our results indicate that the sampling effort is not only remarkable from a taxonomic point of view, with multiple observations for most species, but also for the spatial coverage achieved. The observations are distributed almost continuously across the two-dimensional climatic space of Oman defined by the mean annual temperature and the total annual precipitation and across the Principal Component Analysis (PCA) of the multivariate climatic space and are well represented within 17 out of the 20 climatic clusters grouping 10% of the explained climatic variance defined by PC1 and PC2. Species richness is highest in the Hajar and Dhofar Mountains, two of the most biodiverse areas of the Arabian Peninsula, and endemic species richness is greatest in the Jebel Akhdar, the highest part of the Hajar Mountains. Oman's 22 protected areas cover only 3.91% of the country, including within their limits 63.37% of terrestrial reptiles and 50% of all endemics. Our analyses show that large areas of the climatic space of Oman lie outside protected areas and that seven of the 20 climatic clusters are not protected at all. The results of the gap analysis indicate that most of the species are below the conservation target of 17% or even the less restrictive 12% of their total area within a protected area in order to be considered adequately protected. Therefore, an evaluation of the coverage of the current network of protected areas and the identification of priority protected areas for reptiles using reserve design algorithms are urgently needed. Our study also shows that more than half of the species are still pending of a definitive evaluation by the International Union for Conservation of Nature (IUCN).

Close and distant: Contrasting the metabolism of two closely related subspecies of Scots pine under the effects of folivory and summer drought.

Metabolomes, as chemical phenotypes of organisms, are likely not only shaped by the environment but also by common ancestry. If this is the case, we expect that closely related species of pines will tend to reach similar metabolomic solutions to the same environmental stressors. We examined the metabolomes of two sympatric subspecies of Pinus sylvestris in Sierra Nevada (southern Iberian Peninsula), in summer and winter and exposed to folivory by the pine processionary moth. The overall metabolomes differed between the subspecies but both tended to respond more similarly to folivory. The metabolomes of the subspecies were more dissimilar in summer than in winter, and iberica trees had higher concentrations of metabolites directly related to drought stress. Our results are consistent with the notion that certain plant metabolic responses associated with folivory have been phylogenetically conserved. The larger divergence between subspecies metabolomes in summer is likely due to the warmer and drier conditions that the northern iberica subspecies experience in Sierra Nevada. Our results provide crucial insights into how iberica populations would respond to the predicted conditions of climate change under an increased defoliation in the Mediterranean Basin.

Transcriptomic and macroevolutionary evidence for phenotypic uncoupling between frog life history phases.

Anuran amphibians undergo major morphological transitions during development, but the contribution of their markedly different life-history phases to macroevolution has rarely been analysed. Here we generate testable predictions for coupling versus uncoupling of phenotypic evolution of tadpole and adult life-history phases, and for the underlying expression of genes related to morphological feature formation. We test these predictions by combining evidence from gene expression in two distantly related frogs, Xenopus laevis and Mantidactylus betsileanus, with patterns of morphological evolution in the entire radiation of Madagascan mantellid frogs. Genes linked to morphological structure formation are expressed in a highly phase-specific pattern, suggesting uncoupling of phenotypic evolution across life-history phases. This gene expression pattern agrees with uncoupled rates of trait evolution among life-history phases in the mantellids, which we show to have undergone an adaptive radiation. Our results validate a prevalence of uncoupling in the evolution of tadpole and adult phenotypes of frogs.

Testing the island effect on phenotypic diversification: insights from the Hemidactylus geckos of the Socotra Archipelago.

Island colonization is often assumed to trigger extreme levels of phenotypic diversification. Yet, empirical evidence suggests that it does not always so. In this study we test this hypothesis using a completely sampled mainland-island system, the arid clade of Hemidactylus, a group of geckos mainly distributed across Africa, Arabia and the Socotra Archipelago. To such purpose, we generated a new molecular phylogeny of the group on which we mapped body size and head proportions. We then explored whether island and continental taxa shared the same morphospace and differed in their disparities and tempos of evolution. Insular species produced the most extreme sizes of the radiation, involving accelerated rates of evolution and higher disparities compared with most (but not all) of the continental groups. In contrast, head proportions exhibited constant evolutionary rates across the radiation and similar disparities in islands compared with the continent. These results, although generally consistent with the notion that islands promote high morphological disparity, reveal at the same time a complex scenario in which different traits may experience different evolutionary patterns in the same mainland-island system and continental groups do not always present low levels of morphological diversification compared to insular groups.

Patterns of diversification in islands: A comparative study across three gecko genera in the Socotra Archipelago.

In this study we used the complete fauna of geckos of the Socotra Archipelago to test whether the three gecko genera co-occurring in the islands (Pristurus, Hemidactylus and Haemodracon) produced similar outcomes of morphological and climatic diversification. To test this, we produced a time-calibrated tree of 346 geckos including all 16 endemic species of the archipelago and 26 potential close-relatives in the continent. Our dating estimates revealed that most of the diversity of geckos in the archipelago was the consequence of in situ diversification. However not all genera shared similar patterns of diversification. While in Hemidactylus and Haemodracon this involved great differences in body size and low levels of climatic diversification (mostly involving sympatric distributions), an opposite pattern appeared in Pristurus in which most of the diversification involved shifts in climatic envelopes (mostly involving allopatric and parapatric distributions) but almost no size differentiation. Consistently with this, Pristurus was the only genus in which rates of size diversification in islands were substantially lower than in the continent. This illustrates how different groups can greatly differ in their patterns of intra-island diversification and highlights the importance of taxon-dependent factors at determining different patterns of diversification in the same insular context.