The evolution of targeted cannibalism and cannibal-induced defenses in invasive populations of cane toads.

Biotic conflict can create evolutionary arms races, in which innovation in one group increases selective pressure on another, such that organisms must constantly adapt to maintain the same level of fitness. In some cases, this process is driven by conflict among members of the same species. Intraspecific conflict can be an especially important selective force in high-density invasive populations, which may favor the evolution of strategies for outcompeting or eliminating conspecifics. Cannibalism is one such strategy; by killing and consuming their intraspecific competitors, cannibals enhance their own performance. Cannibalistic behaviors may therefore be favored in invasive populations. Here, we show that cane toad tadpoles (Rhinella marina) from invasive Australian populations have evolved an increased propensity to cannibalize younger conspecifics as well as a unique adaptation to cannibalism-a strong attraction to vulnerable hatchlings-that is absent in the native range. In response, vulnerable conspecifics from invasive populations have evolved both stronger constitutive defenses and greater cannibal-induced plastic responses than their native range counterparts (i.e., rapid prefeeding development and inducible developmental acceleration). These inducible defenses are costly, incurring performance reductions during the subsequent life stage, explaining why plasticity is limited in native populations where hatchlings are not targeted by cannibalistic tadpoles. These results demonstrate the importance of intraspecific conflict in driving rapid evolution, highlight how plasticity can facilitate adaptation following shifts in selective pressure, and show that evolutionary processes can produce mechanisms that regulate invasive populations.

Urbanization and translocation disrupt the relationship between host density and parasite abundance.

The species interactions that structure natural communities are increasingly disrupted by radical habitat change resulting from the widespread processes of urbanization and species translocations. Although many species are disadvantaged by these changes, others thrive in these new environments, achieving densities that exceed those in natural habitats. Often the same species that benefit from urbanization are successful invaders in introduced habitats, suggesting that similar processes promote these species in both environments. Both processes may especially benefit certain species by modifying their interactions with harmful parasites ('enemy release'). To detect such modifications, we first need to identify the mechanisms underlying host-parasite associations in natural populations, then test whether they are disrupted in cities and introduced habitats. We studied the interaction between the cane toad Rhinella marina, a globally invasive species native to South America, and its Amblyomma ticks. Our field study of 642 cane toads across 46 sites within their native range in French Guiana revealed that 56% of toads carried ticks, and that toads with ticks were in poor body condition relative to uninfected conspecifics. Across natural and disturbed habitats tick prevalence and abundance increased with toad density, but this association was disrupted in the urban environment, where tick abundance remained low even where toad densities were high, and prevalence decreased with density. Reductions in the abundance of ticks in urban habitats may be attributable to pesticides (which are sprayed for mosquito control but are also lethal to ticks), and our literature review shows that tick abundance is generally lower in cane toads from urban habitats across South America. In the invasive range, ticks were either absent (in 1,960 toads from Puerto Rico, Hawai'i, Japan and Australia) or less abundant (in Florida and the Caribbean; literature review). The positive relationship between host density and parasite abundance is thought to be a key mechanism through which parasites regulate host populations; anthropogenic processes that disrupt this relationship may allow populations in urban and introduced habitats to persist at densities that would otherwise lead to severe impacts from parasites.

Speed-accuracy trade-off, detour reaching and response to PHA in Carib grackles.

Performance on different cognitive tasks varies between individuals within species. Recent evidence suggests that, in some species, this variation reflects the existence of coherent cognitive strategies bringing together positive and negative relationships between tasks. For example, Carib grackles show a speed-accuracy trade-off, where individuals that are fast at solving novel problems make more errors at discrimination learning than individuals that are slow solvers. Pathogens are thought to play a major role in shaping variation in cognition, either because different cognitive strategies lead to differential exposure to pathogens, or because investment in cognitive abilities is costly, limiting the ability to invest in anti-pathogen responses. In both cases, immunocompetence is expected to co-vary with cognition. Here, using wild-caught Carib grackles, we tested whether performance on reversal learning and detour-reaching tasks is associated with the speed-accuracy trade-off found in a previous study. In parallel, we measured the response of individuals to a phytohemagglutinin (PHA) injection, an immunoecological technique that assesses general immunity. Performance on two problem-solving tasks and two learning tasks was characterized by a speed-accuracy trade-off, reversal learning and discrimination learning performance being better in individuals with slower problem-solving performance. Detour-reaching performance was independent from this trade-off. Finally, our results show that PHA response was higher in accurate but slow grackles, and higher in grackles with better detour-reaching performance. Investigating the emergence and maintenance of variation in cognition in a framework integrating variation in physiology and life history is likely a major step towards a better understanding of the evolution of cognition.

Life-history traits and the fate of translocated populations.

Attempts to identify predictors and mechanisms of invasion success have been weakened by poor data quality, mostly because monitoring does not begin immediately after introduction events. To overcome this issue, we used data from conservation translocations of threatened bird species. We analyzed information on >1200 translocation events of >150 bird species to investigate how life-history traits affect population establishment measured based on rates of survival and reproduction. Species position along the slow-fast life-history continuum was a key predictor of translocation success. Species with fast-paced life histories were less likely to survive (over both short- and mid-term) and more likely to breed successfully than species with slow life histories. The temporal partitioning of reproductive effort (number of clutches per year) also affected the probability of successful reproduction. Our results illustrate how conservation-motivated reintroduction programs can provide proxies for the initial stages of the invasion process, enabling empirical tests of predictions from life-history theory and informing management.

Atributos de las Historias de Vida y el Destino de las Poblaciones Reubicadas Resumen Los intentos por identificar los pronosticadores y los mecanismos del éxito de invasión han sido debilitados por la poca calidad de los datos, principalmente porque el monitoreo no inicia inmediatamente después de los eventos de introducción. Para superar este tema, usamos datos a partir de las reubicaciones por conservación de especies amenazadas de aves. Analizamos la información de más de 1,200 eventos de reubicación para más de 150 especies de aves y así investigar cómo los atributos de las historias de vida afectan el establecimiento de la población medido con base en tasas de supervivencia y reproducción. La posición de las especies a lo largo del continuo de historias de vida lenta-rápida fue un pronosticador importante para el éxito de la reubicación. Las especies con historias de vida rápidas tuvieron una menor posibilidad de sobrevivir (tanto a corto como a mediano plazo) y una mayor probabilidad de reproducirse exitosamente que las especies con historias de vida lentas. La división temporal del esfuerzo reproductivo (número de puestas por año) también afectó la probabilidad del éxito de la reproducción. Nuestros resultados ilustran cómo los programas de reintroducción motivados por la conservación pueden proporcionar sustitutos para los estadios iniciales del proceso de invasión, permitiendo pruebas empíricas a partir de la teoría de la historia de vida e informando a los administradores.

Colour polymorphism is associated with lower extinction risk in birds.

Colour polymorphisms have played a major role in enhancing current understanding of how selection and demography can impact phenotypes. Because different morphs often display alternative strategies and exploit alternative ecological niches, colour polymorphism can be expected to promote adaptability to environmental changes. However, whether and how it could influence populations' and species' response to global changes remains debated. To address this question, we built an up-to-date and complete database on avian colour polymorphism based on the examination of available data from all 10,394 extant bird species. We distinguished between true polymorphism (where different genetically determined morphs co-occur in sympatry within the same population) and geographic variation (parapatric or allopatric colour variation), because these two patterns of variation are expected to have different consequences on populations' persistence. Using the IUCN red list, we then showed that polymorphic bird species are at lesser risk of extinction than nonpolymorphic ones, after controlling for a range of factors such as geographic range size, habitat breadth, life history, and phylogeny. This appears consistent with the idea that high genetic diversity and/or the existence of alternative strategies in polymorphic species promotes the ability to adaptively respond to changing environmental conditions. In contrast, polymorphic species were not less vulnerable than nonpolymorphic ones to specific drivers of extinction such as habitat alteration, direct exploitation, climate change, and invasive species. Thus, our results suggest that colour polymorphism acts as a buffer against environmental changes, although further studies are now needed to understand the underlying mechanisms. Developing accurate quantitative indices of sensitivity to specific threats is likely a key step towards a better understanding of species response to environmental changes.

Innovativeness and the effects of urbanization on risk-taking behaviors in wild Barbados birds.

The effects of urbanization on avian cognition remain poorly understood. Risk-taking behaviors like boldness, neophobia and flight distance are thought to affect opportunism and innovativeness, and should also vary with urbanization. Here, we investigate variation in risk-taking behaviors in the field in an avian assemblage of nine species that forage together in Barbados and for which innovation rate is known from previous work. We predicted that birds from highly urbanized areas would show more risk-taking behavior than conspecifics from less urbanized parts of the island and that the differences would be strongest in the most innovative of the species. Overall, we found that urban birds are bolder, less neophobic and have shorter flight distances than their less urbanized conspecifics. Additionally, we detected between-species differences in the effect of urbanization on flight distance, more innovative species showing smaller differences in flight distance between areas. Our results suggest that, within successful urban colonizers, species differences in innovativeness may affect the way species change their risk-taking behaviors in response to the urban environment.

Evolution of a butterfly dispersal syndrome.

The existence of dispersal syndromes contrasting disperser from resident phenotypes within populations has been intensively documented across taxa. However, how such suites of phenotypic traits emerge and are maintained is largely unknown, although deciphering the processes shaping the evolution of dispersal phenotypes is a key in ecology and evolution. In this study, we created artificial populations of a butterfly, in which we controlled for individual phenotypes and measured experimentally the roles of selection and genetic constraints on the correlations between dispersal-related traits: flight performance and wing morphology. We demonstrate that (i) trait covariations are not due to genetic correlations, (ii) the effects of selection are sex-specific, and (iii) both divergent and stabilizing selection maintain specific flight performance phenotypes and wing morphologies. Interestingly, some trait combinations are also favoured, depending on sex and fitness components. Moreover, we provide evidence for the role of (dis)assortative mating in the evolution of these dispersal-related traits. Our results suggest that dispersal syndromes may have high evolutionary potential, but also that they may be easily disrupted under particular environmental conditions.

Co-adjustment of yolk antioxidants and androgens in birds.

Mothers can shape the developmental trajectory of their offspring through the transmission of resources such as hormones, antioxidants or immunoglobulins. Over the last two decades, an abundant literature on maternal effects in birds has shown that several of these compounds (i.e. androgens, glucocorticoids and antioxidants) often influence the same offspring phenotypic traits (i.e. growth, immunity or oxidative stress levels), making interaction effects between egg components a likely scenario. However, the potential interactive effects of maternally transmitted compounds on offspring development and potential co-adjustment of these compounds within an egg are still poorly understood. Here, we report the results of an interspecific comparative analysis on birds' egg yolk composition (i.e. androgens and antioxidants) where we found that yolk carotenoid and vitamin E concentrations are positively associated, supporting the hypothesis that these two antioxidants act in synergy. The concentrations of vitamin E also increased with increasing concentrations of testosterone. This last result confirms the emerging idea that androgens and antioxidants are co-adjusted within eggs and that maternally transmitted antioxidants might limit the potential direct and indirect effects of prenatal exposure to high testosterone levels on oxidative stress.

Ecological generalism and behavioural innovation in birds: technical intelligence or the simple incorporation of new foods?

Generalist species are more successful than specialists in anthropogenically modified environments or in environments in which they have been introduced, but the nature of the link between generalism and establishment success is unclear. A higher feeding innovation rate has previously been reported in habitat generalist birds from North America. By allowing them to exploit new resources, this higher feeding innovation rate might explain the generalists' advantage. This result might be due to generalists being more likely to find new resources because they are exposed to more diverse environmental conditions. Alternatively, they might differ from specialists in other traits, in particular cognitive skills that might allow them to innovate more complex food searching and handling techniques. To test these hypotheses, we separated avian feeding innovations into a 'technical' (novel searching and handling behaviour) and a 'food type' (incorporation of a new food in a species' diet) category. Technical innovations, but not food type innovations, have previously been shown to correlate with avian brain size, suggesting they reflect cognitive ability. We used a world-wide data base of 2339 feeding innovations recorded in the literature, covering a total of 765 avian species and assessed the correlations between brain size and feeding innovation rates on one side and habitat and diet generalism on the other. Habitat generalism was positively related with food type innovation rate, but not technical innovation rate or brain size. This suggests that habitat generalist species are more likely to incorporate new food types in their diet because of higher chances to find new food resources in their environment, or of a higher opportunism, but not enhanced cognitive skills. In contrast, diet generalist species had higher food type and technical innovation rates, as well as larger brains, suggesting that cognitive skills might help species expand their diet breadth or that an increase in diet breadth might favour the evolution of enhanced cognitive abilities. Our results provide new insights into the nature of the generalists' advantage in the face of environmental changes, and suggest that dietary and habitat generalism are different, but convergent, routes to feeding flexibility and adaptation to changed environments.

Brood parasitism: a good strategy in our changing world?

The original life-history strategy of brood-parasitic birds has been the focus of a large number of studies in ecology and evolution. Whether species adopting such a strategy differ in their response to global changes remains, however, unknown. Both the absence of investment in parental care and the capacity to spread nesting failure by laying eggs in several nests might help brood parasites in dealing with environmental changes. Alternatively, brood parasites might cumulate the negative effects of environmental changes on their own environment and on their hosts' environment. Here, I tested whether brood parasites' extinction risk and population trend differed from those of species with parental care. Focusing on the five bird families containing brood parasite species, I show that brood parasites are less at risk of extinction, and have a more stable population trend than species with parental care. In addition, I found that brood parasites with a higher host diversity were more likely to be increasing than those with fewer hosts. The bet-hedging strategy of brood parasites, by allowing them to spread nesting failure risks associated with environmental changes, is likely to help them resist current global changes.

Morphological and molecular sexing of the monochromatic Barbados bullfinch, Loxigilla barbadensis.

The bullfinch Loxigilla barbadensis is an endemic passerine on the Caribbean island of Barbados that has only recently been taxonomically split from the Lesser Antillean bullfinch L. noctis. The trait that most clearly distinguishes L. barbadensis from L. noctis is the absence in the male of sexually dimorphic coloration of the body and throat feathers, with L. barbadensis males and females sharing the same dull brown plumage. Here we report, in 64 individuals netted throughout the island, the results of a discriminant analysis on two (wing length and tail length) to four morphological traits showing very high (97%) concordance with sexing via PCR using blood samples. Females also show a paler lower mandible, a trait that yields an 80% concordance with PCR sexing. We found one L. barbadensis male that had a noctis-like reddish throat patch, supporting the idea that sexual dichromatism is the ancestral condition and that male Barbados bullfinches have evolved cryptic coloration that now makes the species monochromatic.

Light conditions and the evolution of the visual system in birds.

Despite vision being an essential sense for many animals, the intuitively appealing notion that the visual system has been shaped by environmental light conditions is backed by insufficient evidence. Based on a comprehensive phylogenetic comparative analysis of birds, we investigate if exposure to different light conditions might have triggered evolutionary divergence in the visual system through pressures on light sensitivity, visual acuity, and neural processing capacity. Our analyses suggest that birds that have adopted nocturnal habits evolved eyes with larger corneal diameters and, to a lesser extent, longer axial length than diurnal species. However, we found no evidence that sensing and processing organs were selected together, as observed in diurnal birds. Rather than enlarging the processing centers, we found a tendency among nocturnal species to either reduce or maintain the size of the two main brain centers involved in vision-the optic tectum and the wulst. These results suggest a mosaic pattern of evolution, wherein optimization of the eye optics for efficient light capture in nocturnal species may have compromised visual acuity and central processing capacity.

Whole-mitogenome analysis unveils previously undescribed genetic diversity in cane toads across their invasion trajectory.

Invasive species offer insights into rapid adaptation to novel environments. The iconic cane toad (Rhinella marina) is an excellent model for studying rapid adaptation during invasion. Previous research using the mitochondrial NADH dehydrogenase 3 (ND3) gene in Hawai'ian and Australian invasive populations found a single haplotype, indicating an extreme genetic bottleneck following introduction. Nuclear genetic diversity also exhibited reductions across the genome in these two populations. Here, we investigated the mitochondrial genomics of cane toads across this invasion trajectory. We created the first reference mitochondrial genome for this species using long-read sequence data. We combined whole-genome resequencing data of 15 toads with published transcriptomic data of 125 individuals to construct nearly complete mitochondrial genomes from the native (French Guiana) and introduced (Hawai'i and Australia) ranges for population genomic analyses. In agreement with previous investigations of these populations, we identified genetic bottlenecks in both Hawai'ian and Australian introduced populations, alongside evidence of population expansion in the invasive ranges. Although mitochondrial genetic diversity in introduced populations was reduced, our results revealed that it had been underestimated: we identified 45 mitochondrial haplotypes in Hawai'ian and Australian samples, none of which were found in the native range. Additionally, we identified two distinct groups of haplotypes from the native range, separated by a minimum of 110 base pairs (0.6%). These findings enhance our understanding of how invasion has shaped the genetic landscape of this species.

Intra- and inter-individual variation in flight direction in a migratory butterfly co-vary with individual mobility.

Flight direction is a major component of an animal's migratory success. However, few studies have focused on variation in flight direction both between and within individuals, which is likely to be correlated with other traits implied in migration processes. We report patterns of intra- and inter-individual variation in flight direction in the large white butterfly Pieris brassicae. The presence of inter-individual variation in flight direction for individuals tested in the same conditions suggests that this trait is inherited in P. brassicae and we propose that a rapid loss of migratory skills may exist in the absence of selection for migration. The magnitude of intra-individual variation was negatively correlated to two surrogates of the potential for migration: mobility and wing length. Highly mobile and longed-winged individuals within the same family were found to fly in similar directions, whereas less mobile and short-winged individuals displayed divergent flight direction compared with the average direction of their kin. There was also a negative correlation between the variance to the mean flight direction of a family and its average mobility, but no correlation with wing length. We discuss these issues in terms of the evolution of traits potentially implied in both migration and dispersal in P. brassicae.

Population sex ratio and dispersal in experimental, two-patch metapopulations of butterflies.

1. Sex-biased dispersal, that is, the difference in dispersal between males and females, is thought to be the consequence of any divergent evolutionary responses between sexes. In anisogamous species, asymmetry in parental investment may lead to sexual conflict, which entails male-male competition (for sexual partner access), female-female competition (for feeding or egg-laying habitat patches) and/or male-female competition (antagonistic co-evolution). 2. As competition is one of the main causes of dispersal evolution, intra- and intersexual competition should have strong consequences on sex-biased dispersal. However, very few experimental studies, if any, have simultaneously addressed the effect of biased sex ratio on (i) each dispersal stage (emigration, transience, immigration), (ii) the dispersal phenotype and (iii) the colonization success of new habitat in order to fully separate the effects of varying male and female density. 3. Here, we used the Metatron, a unique experimental system composed of 48 interconnected enclosed patches dedicated to the study of dispersal in meta-ecosystems, to investigate the effect of sex ratio on dispersal in a butterfly. We created six populations with three different sex ratios in pairs of patches and recorded individual movements in these simple metapopulations. 4. Emigration was higher when the proportion of males was higher, and individuals reached the empty patch at a higher rate when the sex ratio in the departure patch was balanced. Males had a better dispersal success than females, which had a lower survival rate during dispersal and after colonization. We also showed that sex and wing size are major components of the dispersal response. 5. We did not observe sex-biased dispersal; our results thus suggest that female harassment by males and male-male competition might be more important mechanisms for the dispersal of females and males, than the search for a mating partner. Furthermore, the demonstration of a differential mortality between males and females during dispersal provides causal hypotheses of the evolution of sex-biased dispersal.

European birds adjust their flight initiation distance to road speed limits.

Behavioural responses can help species persist in habitats modified by humans. Roads and traffic greatly affect animals' mortality not only through habitat structure modifications but also through direct mortality owing to collisions. Although species are known to differ in their sensitivity to the risk of collision, whether individuals can change their behaviour in response to this is still unknown. Here, we tested whether common European birds changed their flight initiation distances (FIDs) in response to vehicles according to road speed limit (a known factor affecting killing rates on roads) and vehicle speed. We found that FID increased with speed limit, although vehicle speed had no effect. This suggests that birds adjust their flight distance to speed limit, which may reduce collision risks and decrease mortality maximizing the time allocated to foraging behaviours. Mobility and territory size are likely to affect an individuals' ability to respond adaptively to local speed limits.

Oxidative physiology is weakly associated with pigmentation in birds.

The mechanistic link between avian oxidative physiology and plumage coloration has attracted considerable attention in past decades. Hence, multiple proximal hypotheses were proposed to explain how oxidative state might covary with the production of melanin and carotenoid pigments. Some hypotheses underscore that these pigments (or their precursors, e.g., glutathione) have antioxidant capacities or function as molecules storing the toxic excess of intracellular compounds, while others highlight that these pigments can act as pro-oxidants under specific conditions. Most studies addressing these associations are at the intraspecific level, while phylogenetic comparative studies are still scarce, though needed to assess the generality of these associations. Here, we tested whether plumage and bare part coloration were related to oxidative physiology at an interspecific level by measuring five oxidative physiology markers (three nonenzymatic antioxidants and two markers of lipid peroxidative damage) in 1387 individuals of 104 European bird species sampled during the breeding season, and by scoring plumage eumelanin, pheomelanin, and carotenoid content for each sex and species. Only the plasma level of reactive oxygen metabolites was related to melanin coloration, being positively associated with eumelanin score and negatively with pheomelanin score. Thus, our results do not support the role of antioxidant glutathione in driving variation in melanin synthesis across species. Furthermore, the carotenoid scores of feathers and bare parts were unrelated to the measured oxidative physiology parameters, further suggesting that the marked differences in pigmentation across birds does not influence their oxidative state.

Disentangling the avian altricial-precocial spectrum: Quantitative assessment of developmental mode, phylogenetic signal, and dimensionality.

The altricial-precocial spectrum describes patterns of variation in avian developmental mode that greatly influence avian life histories. Appraising a given species' position on this spectrum is therefore fundamental to understanding patterns of avian life history evolution. However, evaluating avian developmental mode remains a relatively subjective task reliant on untested assumptions, including the notion that developmental strategies are distributed along a single dimension of statistical variation. Here, we present a quantitative multivariate framework that objectively discriminates among meaningfully different modes of avian development. We gathered information on seven hatchling and post-hatching traits for up to 4000 extant bird species, and find that most traits related to developmental mode show high phylogenetic signal and little intraclade variation, allowing unknown values to be reliably interpolated. Principal component analyses (PCAs) of these traits illustrate that most variation in hatchling state can be quantified along one dimension of trait space. However, our PCAs also reveal an important second dimension explaining variation in post-hatching behavior, enabling factors related to hatchling state and post-hatching behavior to be disentangled. In order to facilitate future macroevolutionary studies of variation in avian developmental strategies, as well as explorations of covariation between developmental mode and other aspects of avian biology, we present PC scores for 9993 extant avian species.

Spatial ecology of cane toads (Rhinella marina) in their native range: a radiotelemetric study from French Guiana.

Like most invasive species, cane toads have attracted less research in their native range than in invaded areas. We radio-tracked 34 free-ranging toads in French Guiana, a source region for most invasive populations, across two coastal and two rainforest sites. Coastal toads generally sheltered in pools of fresh or brackish water but nocturnally foraged on beaches, whereas rainforest toads sheltered in forested habitats, moving into open areas at night. Over five days of monitoring, native toads frequently re-used shelters and moved little between days (means = 10-63 m/site) compared to invasion-front toads from Australia (~ 250 m). Larger toads moved less between days, but displaced in more consistent directions. At night, foraging toads travelled up to 200 m before returning to shelters. Foraging distance was related to body condition at coastal sites, with toads in poorer body condition travelling farther. Rain increased the probability of coastal toads sheltering in the dry habitats where they foraged. Dispersal and rainfall were lower at coastal sites, and the strategies utilized by coastal toads to minimize water loss resembled those of invasive toads in semi-desert habitats. This global invader already exhibits a broad environmental niche and substantial behavioural flexibility within its native range.

Increased rates of dispersal of free-ranging cane toads (Rhinella marina) during their global invasion.

Invasions often accelerate through time, as dispersal-enhancing traits accumulate at the expanding range edge. How does the dispersal behaviour of individual organisms shift to increase rates of population spread? We collate data from 44 radio-tracking studies (in total, of 650 animals) of cane toads (Rhinella marina) to quantify distances moved per day, and the frequency of displacement in their native range (French Guiana) and two invaded areas (Hawai'i and Australia). We show that toads in their native-range, Hawai'i and eastern Australia are relatively sedentary, while toads dispersing across tropical Australia increased their daily distances travelled from 20 to 200 m per day. That increase reflects an increasing propensity to change diurnal retreat sites every day, as well as to move further during each nocturnal displacement. Daily changes in retreat site evolved earlier than did changes in distances moved per night, indicating a breakdown in philopatry before other movement behaviours were optimised to maximise dispersal.