Many insular taxa possess extraordinary abilities to disperse but may differ in their abilities to diversify and compete. While some taxa are widespread across archipelagos, others have disjunct (relictual) populations. These types of taxa, exemplified in the literature by selections of unrelated taxa, have been interpreted as representing a continuum of expansions and contractions (i.e. taxon cycles). Here, we use molecular data of 35 out of 40 species of the avian genus Pachycephala (including 54 out of 66 taxa in Pachycephala pectoralis (sensu lato), to assess the spatio-temporal evolution of the group. We also include data on species distributions, morphology, habitat and elevational ranges to test a number of predictions associated with the taxon-cycle hypothesis. We demonstrate that relictual species persist on the largest and highest islands across the Indo-Pacific, whereas recent archipelago expansions resulted in colonization of all islands in a region. For co-occurring island taxa, the earliest colonists generally inhabit the interior and highest parts of an island, with little spatial overlap with later colonists. Collectively, our data support the idea that taxa continuously pass through phases of expansions and contractions (i.e. taxon cycles).
Australo-Papua; coexistence; community assembly; island biogeography; molecular phylogeny; Wallacea
When opposing evolutionary selection pressures act on a behavioural trait, the result is often stabilizing selection for an intermediate optimal phenotype, with deviations from the predicted optimum attributed to tracking a moving target, development of behavioural syndromes or shifts in riskiness over an individual's lifetime. We investigated nest-site choice by female golden-winged warblers, and the selection pressures acting on that choice by two fitness components, nest success and fledgling survival. We observed strong and consistent opposing selection pressures on nest-site choice for maximizing these two fitness components, and an abrupt, within-season switch in the fitness component birds prioritize via nest-site choice, dependent on the time remaining for additional nesting attempts. We found that females consistently deviated from the predicted optimal behaviour when choosing nest sites because they can make multiple attempts at one fitness component, nest success, but only one attempt at the subsequent component, fledgling survival. Our results demonstrate a unique natural strategy for balancing opposing selection pressures to maximize total fitness. This time-dependent switch from high to low risk tolerance in nest-site choice maximizes songbird fitness in the same way a well-timed switch in human investor risk tolerance can maximize one's nest egg at retirement. Our results also provide strong evidence for the adaptive nature of songbird nest-site choice, which we suggest has been elusive primarily due to a lack of consideration for fledgling survival.
avian productivity; fitness; fledgling; nest success; stabilizing selection; Vermivora chrysoptera
The ‘diversity–stability hypothesis’, in which higher species diversity within biological communities buffers the risk of ecological collapse, is now generally accepted. However, empirical evidence for a relationship between β-diversity (spatial turnover in community structure) and temporal stability in community structure remains equivocal, despite important implications for theoretical ecology and conservation biology. Here, we report strong β-diversity–stability relationships across a broad sample of fish taxa on Australia's Great Barrier Reef. These relationships were robust to random sampling error and spatial and environmental factors, such as latitude, reef size and isolation. While β-diversity was positively associated with temporal stability at the community level, the relationship was negative for some taxa, for example surgeonfishes (Acanthuridae), one of the most abundant reef fish families. This demonstrates that the β-diversity–stability relationship should not be indiscriminately assumed for all taxa, but that a species’ risk of extirpation in response to disturbance is likely to be taxon specific and trait based. By combining predictions of spatial and temporal turnover across the study area with observations in marine-protected areas, we conclude that protection alone does not necessarily confer temporal stability and that taxon-specific considerations will improve the outcome of conservation efforts.
β-diversity; Bray–Curtis; disturbance; long-term monitoring; mantel; time series
The addition of spatial structure to ecological concepts and theories has spurred integration between sub-disciplines within ecology, including community and ecosystem ecology. However, the complexity of spatial models limits their implementation to idealized, regular landscapes. We present a model meta-ecosystem with finite and irregular spatial structure consisting of local nutrient–autotrophs–herbivores ecosystems connected through spatial flows of materials and organisms. We study the effect of spatial flows on stability and ecosystem functions, and provide simple metrics of connectivity that can predict these effects. Our results show that high rates of nutrient and herbivore movement can destabilize local ecosystem dynamics, leading to spatially heterogeneous equilibria or oscillations across the meta-ecosystem, with generally increased meta-ecosystem primary and secondary production. However, the onset and the spatial scale of these emergent dynamics depend heavily on the spatial structure of the meta-ecosystem and on the relative movement rate of the autotrophs. We show how this strong dependence on finite spatial structure eludes commonly used metrics of connectivity, but can be predicted by the eigenvalues and eigenvectors of the connectivity matrix that describe the spatial structure and scale. Our study indicates the need to consider finite-size ecosystems in meta-ecosystem theory.
meta-ecosystem; networks; connectivity; movement; ecosystem functioning; ecosystem dynamics
The jump–yip display of black-tailed prairie dogs (Cynomys ludovicianus) is contagious, spreading through a prairie dog town as ‘the wave’ through a stadium. Because contagious communication in primates serves to assess conspecific social awareness, we investigated whether instigators of jump–yip bouts adjusted their behaviour relative to the response of conspecifics recruited to display bouts. Increased responsiveness of neighbouring town members resulted in bout initiators devoting a significantly greater proportion of time to active foraging. Contagious jump–yips thus function to assess neighbours’ alertness, soliciting social information to assess effective conspecific group size in real time and reveal active probing of conspecific awareness consistent with theory of mind in these group-living rodents.
contagious communication; group-size effect; public information; theory of mind; foraging–vigilance trade-off; prairie dogs
The rate of DNA mutation and divergence is highly variable across the tree of life. However, the reasons underlying this variation are not well understood. Comparing the rates of genetic changes between hosts and parasite lineages that diverged at the same time is one way to begin to understand differences in genetic mutation and substitution rates. Such studies have indicated that the rate of genetic divergence in parasites is often faster than that of their hosts when comparing single genes. However, the variation in this relative rate of molecular evolution across different genes in the genome is unknown. We compared the rate of DNA sequence divergence between humans, chimpanzees and their ectoparasitic lice for 1534 protein-coding genes across their genomes. The rate of DNA substitution in these orthologous genes was on average 14 times faster for lice than for humans and chimpanzees. In addition, these rates were positively correlated across genes. Because this correlation only occurred for substitutions that changed the amino acid, this pattern is probably produced by similar functional constraints across the same genes in humans, chimpanzees and their ectoparasites.
coevolution; genomics; molecular evolution; hosts and parasites; Pediculus
Rising CO2 levels in the oceans are predicted to have serious consequences for many marine taxa. Recent studies suggest that non-genetic parental effects may reduce the impact of high CO2 on the growth, survival and routine metabolic rate of marine fishes, but whether the parental environment mitigates behavioural and sensory impairment associated with high CO2 remains unknown. Here, we tested the acute effects of elevated CO2 on the escape responses of juvenile fish and whether such effects were altered by exposure of parents to increased CO2 (transgenerational acclimation). Elevated CO2 negatively affected the reactivity and locomotor performance of juvenile fish, but parental exposure to high CO2 reduced the effects in some traits, indicating the potential for acclimation of behavioural impairment across generations. However, acclimation was not complete in some traits, and absent in others, suggesting that transgenerational acclimation does not completely compensate the effects of high CO2 on escape responses.
climate change; carbon dioxide; ocean acidification; acclimation predation; locomotion; parental effects
Exploring the ability of organisms to locally adapt is critical for determining the outcome of rapid climate changes, yet few studies have addressed this question in microorganisms. We investigated the role of a heterogeneous climate on adaptation of North American populations of the wild yeast Saccharomyces paradoxus. We found abundant among-strain variation for fitness components across a range of temperatures, but this variation was only partially explained by climatic variation in the distribution area. Most of fitness variation was explained by the divergence of genetically distinct groups, distributed along a north–south cline, suggesting that these groups have adapted to distinct climatic conditions. Within-group fitness components were correlated with climatic conditions, illustrating that even ubiquitous microorganisms locally adapt and harbour standing genetic variation for climate-related traits. Our results suggest that global climatic changes could lead to adaptation to new conditions within groups, or changes in their geographical distributions.
Saccharomyces paradoxus; climate adaptation; global warming; temperature-dependent fitness; freeze–thaw survival
The extent and intensity of pre-Columbian impacts on lowland Amazonia have remained uncertain and controversial. Various indicators can be used to gauge the impact of pre-Columbian societies, but the formation of nutrient-enriched terra preta soils has been widely accepted as an indication of long-term settlement and site fidelity. Using known and newly discovered terra preta sites and maximum entropy algorithms (Maxent), we determined the influence of regional environmental conditions on the likelihood that terra pretas would have been formed at any given location in lowland Amazonia. Terra pretas were most frequently found in central and eastern Amazonia along the lower courses of the major Amazonian rivers. Terrain, hydrologic and soil characteristics were more important predictors of terra preta distributions than climatic conditions. Our modelling efforts indicated that terra pretas are likely to be found throughout ca 154 063 km2 or 3.2% of the forest. We also predict that terra preta formation was limited in most of western Amazonia. Model results suggested that the distribution of terra preta was highly predictable based on environmental parameters. We provided targets for future archaeological surveys under the vast forest canopy and also highlighted how few of the long-term forest inventory sites in Amazonia are able to capture the effects of historical disturbance.
Amazonia; anthrosols; maxent algorithms; modified soils; pre-Columbian impacts; terra preta
Communication is a characteristic of life, but its reliability and basic definition are hotly debated. Theory predicts that trade among mutualists requires high reliability. Here, we show that moderate reliability already allows mutualists to optimize their rewards. The colours of Mediterranean fleshy-fruits indicate lipid rewards (but not other nutrients) to avian seed dispersers on regional and local scales. On the regional scale, fruits with high lipid content were significantly darker and less chromatic than congeners with lower lipid content. On the local scale, two warbler species (Sylvia atricapilla and Sylvia borin) selected fruit colours that were less chromatic, and thereby maximized their intake of lipids—a critical resource during migration and wintering. Crucially, birds were able to maximize lipid rewards with moderate reliability from visual fruit colours (r2 = 0.44–0.60). We suggest that mutualisms require only that any association between the quality and sensory aspects of signallers is learned through multiple, repeated interactions. Because these conditions are often fulfilled, also in social communication systems, we contend that selection on reliability is less intense than hitherto assumed. This may contribute to explaining the extraordinary diversity of signals, including that of plant reproductive displays.
communication; mutualism; seed dispersal; honest signalling; signal theory; sensory ecology
Many seaweeds and terrestrial plants induce chemical defences in response to herbivory, but whether they induce chemical defences against competitors (allelopathy) remains poorly understood. We evaluated whether two tropical seaweeds induce allelopathy in response to competition with a reef-building coral. We also assessed the effects of competition on seaweed growth and seaweed chemical defence against herbivores. Following 8 days of competition with the coral Porites cylindrica, the chemically rich seaweed Galaxaura filamentosa induced increased allelochemicals and became nearly twice as damaging to the coral. However, it also experienced significantly reduced growth and increased palatability to herbivores (because of reduced chemical defences). Under the same conditions, the seaweed Sargassum polycystum did not induce allelopathy and did not experience a change in growth or palatability. This is the first demonstration of induced allelopathy in a seaweed, or of competitors reducing seaweed chemical defences against herbivores. Our results suggest that the chemical ecology of coral–seaweed–herbivore interactions can be complex and nuanced, highlighting the need to incorporate greater ecological complexity into the study of chemical defence.
chemical ecology; coral reef; Fiji; herbivory; inducible defence; macroalgae
In Italy, during the course of the past century to the present-day, measles incidence underwent a remarkable decreasing trend that started well before the introduction of the national immunization programme. In this work, we aim at examining to what extent both the demographic transition, characterized by declining mortality and fertility rates over time, and the vaccination programme are responsible for the observed epidemiological pattern. Making use of a non-stationary, age-structured disease transmission model, we show that in the pre-vaccination era, from 1901 to 1982, the decline in birth rates has resulted in a drastic decrease in the effective transmission rate, which in turn has determined a declining trend of measles incidence (from 25.2 to 10.3 infections per 1000 individuals). However, since 1983, vaccination appears to have become the major contributing factor in the decrease of measles incidence, which otherwise would have remained stable as a consequence of the nearly constant birth rates. This led to a remarkable decrease in the effective transmission rate, to a level well below the critical threshold for disease persistence. These findings call for the adoption of epidemiological models, which deviate the age structure from stationary equilibrium solutions, to better understand the biology of infectious diseases and evaluate immunization programmes.
infectious diseases; demography; population dynamics
Trade-offs arise when two functional traits impose conflicting demands on the same design trait. Consequently, excellence in one comes at the cost of performance in the other. One of the most widely studied performance trade-offs is the one between sprint speed and endurance. Although biochemical, physiological and (bio)mechanical correlates of either locomotor trait conflict with each other, results at the whole-organism level are mixed. Here, we test whether burst (speed, acceleration) and sustained locomotion (stamina) trade off at both the isolated muscle and whole-organism level among 17 species of lacertid lizards. In addition, we test for a mechanical link between the organismal and muscular (power output, fatigue resistance) performance traits. We find weak evidence for a trade-off between burst and sustained locomotion at the whole-organism level; however, there is a significant trade-off between muscle power output and fatigue resistance in the isolated muscle level. Variation in whole-animal sprint speed can be convincingly explained by variation in muscular power output. The variation in locomotor stamina at the whole-organism level does not relate to the variation in muscle fatigue resistance, suggesting that whole-organism stamina depends not only on muscle contractile performance but probably also on the performance of the circulatory and respiratory systems.
trade-off; locomotion; whole-organism; muscle
Statistical species delimitation usually relies on singular data, primarily genetic, for detecting putative species and individual assignment to putative species. Given the variety of speciation mechanisms, singular data may not adequately represent the genetic, morphological and ecological diversity relevant to species delimitation. We describe a methodological framework combining multivariate and clustering techniques that uses genetic, morphological and ecological data to detect and assign individuals to putative species. Our approach recovers a similar number of species recognized using traditional, qualitative taxonomic approaches that are not detected when using purely genetic methods. Furthermore, our approach detects groupings that traditional, qualitative taxonomic approaches do not. This empirical test suggests that our approach to detecting and assigning individuals to putative species could be useful in species delimitation despite varying levels of differentiation across genetic, phenotypic and ecological axes. This work highlights a critical, and often overlooked, aspect of the process of statistical species delimitation—species detection and individual assignment. Irrespective of the species delimitation approach used, all downstream processing relies on how individuals are initially assigned, and the practices and statistical issues surrounding individual assignment warrant careful consideration.
ecology; individual assignment; morphology; multilocus genetics; species delimitation; species detection
One of the grand goals of historical biogeography is to understand how and why species' population sizes and distributions change over time. Multiple types of data drawn from disparate fields, combined into a single modelling framework, are necessary to document changes in a species's demography and distribution, and to determine the drivers responsible for change. Yet truly integrated approaches are challenging and rarely performed. Here, we discuss a modelling framework that integrates spatio-temporal fossil data, ancient DNA, palaeoclimatological reconstructions, bioclimatic envelope modelling and coalescence models in order to statistically test alternative hypotheses of demographic and potential distributional changes for the iconic American bison (Bison bison). Using different assumptions about the evolution of the bioclimatic niche, we generate hypothetical distributional and demographic histories of the species. We then test these demographic models by comparing the genetic signature predicted by serial coalescence against sequence data derived from subfossils and modern populations. Our results supported demographic models that include both climate and human-associated drivers of population declines. This synthetic approach, integrating palaeoclimatology, bioclimatic envelopes, serial coalescence, spatio-temporal fossil data and heterochronous DNA sequences, improves understanding of species' historical biogeography by allowing consideration of both abiotic and biotic interactions at the population level.
ancient DNA; bison; bioclimatic envelope models; Late Quaternary; historical biogeography; palaeoclimatic reconstructions
In mammals, the mass-specific rate of biomass production during gestation and lactation, here called maternal productivity, has been shown to vary with body size and lifestyle. Metabolic theory predicts that post-weaning growth of offspring, here termed juvenile productivity, should be higher than maternal productivity, and juveniles of smaller species should be more productive than those of larger species. Furthermore because juveniles generally have similar lifestyles to their mothers, across species juvenile and maternal productivities should be correlated. We evaluated these predictions with data from 270 species of placental mammals in 14 taxonomic/lifestyle groups. All three predictions were supported. Lagomorphs, perissodactyls and artiodactyls were very productive both as juveniles and as mothers as expected from the abundance and reliability of their foods. Primates and bats were unproductive as juveniles and as mothers, as expected as an indirect consequence of their low predation risk and consequent low mortality. Our results point the way to a mechanistic explanation for the suite of correlated life-history traits that has been called the slow–fast continuum.
life history; slow–fast continuum; metabolic ecology; allometry; scaling
Species with broad ecological amplitudes with respect to a key focal resource, niche generalists, should maintain larger and more connected populations than niche specialists, leading to the prediction that nucleotide diversity will be lower and more subdivided in specialists relative to their generalist relatives. This logic describes the specialist-generalist variation hypothesis (SGVH). Some outbreeding species of Caenorhabditis nematodes use a variety of invertebrate dispersal vectors and have high molecular diversity. By contrast, Caenorhabditis japonica lives in a strict association and synchronized life cycle with its dispersal host, the shield bug Parastrachia japonensis, itself a diet specialist. Here, we characterize sequence variation for 20 nuclear loci to investigate how C. japonica's life history shapes nucleotide diversity. We find that C. japonica has more than threefold lower polymorphism than other outbreeding Caenorhabditis species, but that local populations are not genetically disconnected. Coupled with its restricted range, we propose that its specialist host association contributes to a smaller effective population size and lower genetic variation than host generalist Caenorhabditis species with outbreeding reproductive modes. A literature survey of diverse organisms provides broader support for the SGVH. These findings encourage further testing of ecological and evolutionary hypotheses with comparative population genetics in Caenorhabditis and other taxa.
Caenorhabditis; specialists; generalists; niche; phoresy; Parastrachia
Marine protected areas (MPAs) are key tools for combatting the global overexploitation of endangered species. The prevailing paradigm is that MPAs are beneficial in helping to restore ecosystems to more ‘natural’ conditions. However, MPAs may have unintended negative effects when increasing densities of protected species exert destructive effects on their habitat. Here, we report on severe seagrass degradation in a decade-old MPA where hyper-abundant green turtles adopted a previously undescribed below-ground foraging strategy. By digging for and consuming rhizomes and roots, turtles create abundant bare gaps, thereby enhancing erosion and reducing seagrass regrowth. A fully parametrized model reveals that the ecosystem is approaching a tipping point, where consumption overwhelms regrowth, which could potentially lead to complete collapse of the seagrass habitat. Seagrass recovery will not ensue unless turtle density is reduced to nearly zero, eliminating the MPA's value as a turtle reserve. Our results reveal an unrecognized, yet imminent threat to MPAs, as sea turtle densities are increasing at major nesting sites and the decline of seagrass habitat forces turtles to concentrate on the remaining meadows inside reserves. This emphasizes the need for policy and management approaches that consider the interactions of protected species with their habitat.
marine reserves; plant–herbivore interactions; alternate stable states
The trajectory of an animal's growth in early development has been shown to have long-term effects on a range of life-history traits. Although it is known that individual differences in behaviour may also be related to certain life-history traits, the linkage between early growth or development and individual variation in behaviour has received little attention. We used brief temperature manipulations, independent of food availability, to stimulate compensatory growth in juvenile three-spined sticklebacks Gasterosteus aculeatus. Here, we examine how these manipulated growth trajectories affected the sexual responsiveness of the male fish at the time of sexual maturation, explore associations between reproductive behaviour and investment and lifespan and test whether the perceived time stress (until the onset of the breeding season) influenced such trade-offs. We found a negative impact of growth rate on sexual responsiveness: fish induced (by temperature manipulation) to grow slowest prior to the breeding season were consistently quickest to respond to the presence of a gravid female. This speed of sexual responsiveness was also positively correlated with the rate of development of sexual ornaments and time taken to build a nest. However, after controlling for effects of growth rate, those males that had the greatest sexual responsiveness to females had the shortest lifespan. Moreover, the time available to compensate in size before the onset of the breeding season (time stress) affected the magnitude of these effects. Our results demonstrate that developmental perturbations in early life can influence mating behaviour, with long-term effects on longevity.
compensatory growth; longevity; trade-off; phenotypic plasticity; sexual behaviour; three-spined stickleback
Atlantic cod (Gadus morhua) vertebrae from archaeological sites were used to study the history of the Icelandic Atlantic cod population in the time period of 1500–1990. Specifically, we used coalescence modelling to estimate population size and fluctuations from the sequence diversity at the cytochrome b (cytb) and Pantophysin I (PanI) loci. The models are consistent with an expanding population during the warm medieval period, large historical effective population size (NE), a marked bottleneck event at 1400–1500 and a decrease in NE in early modern times. The model results are corroborated by the reduction of haplotype and nucleotide variation over time and pairwise population distance as a significant portion of nucleotide variation partitioned across the 1550 time mark. The mean age of the historical fished stock is high in medieval times with a truncation in age in early modern times. The population size crash coincides with a period of known cooling in the North Atlantic, and we conclude that the collapse may be related to climate or climate-induced ecosystem change.
Atlantic cod; coalescence modelling; ancient DNA; effective population size
Most known starfish species possess a compound eye at the tip of each arm, which, except for the lack of true optics, resembles an arthropod compound eye. Although these compound eyes have been known for about two centuries, no visually guided behaviour has ever been directly associated with their presence. There are indications that they are involved in negative phototaxis but this may also be governed by extraocular photoreceptors. Here, we show that the eyes of the coral-reef-associated starfish Linckia laevigata are slow and colour blind. The eyes are capable of true image formation although with low spatial resolution. Further, our behavioural experiments reveal that only specimens with intact eyes can navigate back to their reef habitat when displaced, demonstrating that this is a visually guided behaviour. This is, to our knowledge, the first report of a function of starfish compound eyes. We also show that the spectral sensitivity optimizes the contrast between the reef and the open ocean. Our results provide an example of an eye supporting only low-resolution vision, which is believed to be an essential stage in eye evolution, preceding the high-resolution vision required for detecting prey, predators and conspecifics.
echinoderm; Linckia; compound eye; coral reef; navigation
One of Darwin's most widely known conjectures is that prey are tame on remote islands, where mammalian predators are absent. Many species appear to permit close approach on such islands, but no comparative studies have demonstrated reduced wariness quantified as flight initiation distance (FID; i.e. predator–prey distance when the prey begins to flee) in comparison with mainland relatives. We used the phylogenetic comparative method to assess influence of distance from the mainland and island area on FID of 66 lizard species. Because body size and predator approach speed affect predation risk, we included these as independent variables. Multiple regression showed that FID decreases as distance from mainland increases and is shorter in island than mainland populations. Although FID increased as area increased in some models, collinearity made it difficult to separate effects of area from distance and island occupancy. FID increases as SVL increases and approach speed increases; these effects are statistically independent of effects of distance to mainland and island occupancy. Ordinary least-squares models fit the data better than phylogenetic regressions, indicating little or no phylogenetic signal in residual FID after accounting for the independent variables. Our results demonstrate that island tameness is a real phenomenon in lizards.
antipredatory behaviour; body size; escape behaviour; flight initiation distance; island tameness; lizard