Showing papers in "Biological Reviews in 2019"

Emerging threats and persistent conservation challenges for freshwater biodiversity

Abstract: In the 12 years since Dudgeon et al. (2006) reviewed major pressures on freshwater ecosystems, the biodiversity crisis in the world’s lakes, reservoirs, rivers, streams and wetlands has deepened. While lakes, reservoirs and rivers cover only 2.3% of the Earth’s surface, these ecosystems host at least 9.5% of the Earth’s described animal species. Furthermore, using the World Wide Fund for Nature’s Living Planet Index, freshwater population declines (83% between 1970 and 2014) continue to outpace contemporaneous declines in marine or terrestrial systems. The Anthropocene has brought multiple new and varied threats that disproportionately impact freshwater systems. We document 12 emerging threats to freshwater biodiversity that are either entirely new since 2006 or have since intensified: (i) changing climates; (ii) e-commerce and invasions; (iii) infectious diseases; (iv) harmful algal blooms; (v) expanding hydropower; (vi) emerging contaminants; (vii) engineered nanomaterials; (viii) microplastic pollution; (ix) light and noise; (x) freshwater salinisation; (xi) declining calcium; and (xii) cumulative stressors. Effects are evidenced for amphibians, fishes, invertebrates, microbes, plants, turtles and waterbirds, with potential for ecosystem-level changes through bottom-up and top-down processes. In our highly uncertain future, the net effects of these threats raise serious concerns for freshwater ecosystems. However, we also highlight opportunities for conservation gains as a result of novel management tools (e.g. environmental flows, environmental DNA) and specific conservation-oriented actions (e.g. dam removal, habitat protection policies,managed relocation of species) that have been met with varying levels of success.Moving forward, we advocate hybrid approaches that manage fresh waters as crucial ecosystems for human life support as well as essential hotspots of biodiversity and ecological function. Efforts to reverse global trends in freshwater degradation now depend on bridging an immense gap between the aspirations of conservation biologists and the accelerating rate of species endangerment.

Analysing ecological networks of species interactions.

Abstract: Network approaches to ecological questions have been increasingly used, particularly in recent decades. The abstraction of ecological systems - such as communities - through networks of interactions between their components indeed provides a way to summarize this information with single objects. The methodological framework derived from graph theory also provides numerous approaches and measures to analyze these objects and can offer new perspectives on established ecological theories as well as tools to address new challenges. However, prior to using these methods to test ecological hypotheses, it is necessary that we understand, adapt, and use them in ways that both allow us to deliver their full potential and account for their limitations. Here, we attempt to increase the accessibility of network approaches by providing a review of the tools that have been developed so far, with - what we believe to be - their appropriate uses and potential limitations. This is not an exhaustive review of all methods and metrics, but rather, an overview of tools that are robust, informative, and ecologically sound. After providing a brief presentation of species interaction networks and how to build them in order to summarize ecological information of different types, we then classify methods and metrics by the types of ecological questions that they can be used to answer from global to local scales, including methods for hypothesis testing and future perspectives. Specifically, we show how the organization of species interactions in a community yields different network structures (e.g., more or less dense, modular or nested), how different measures can be used to describe and quantify these emerging structures, and how to compare communities based on these differences in structures. Within networks, we illustrate metrics that can be used to describe and compare the functional and dynamic roles of species based on their position in the network and the organization of their interactions as well as associated new methods to test the significance of these results. Lastly, we describe potential fruitful avenues for new methodological developments to address novel ecological questions.

Resilience and restoration of tropical and subtropical grasslands, savannas, and grassy woodlands.

Abstract: Despite growing recognition of the conservation values of grassy biomes, our understanding of how to maintain and restore biodiverse tropical grasslands (including savannas and open-canopy grassy woodlands) remains limited. To incorporate grasslands into large-scale restoration efforts, we synthesised existing ecological knowledge of tropical grassland resilience and approaches to plant community restoration. Tropical grassland plant communities are resilient to, and often dependent on, the endogenous disturbances with which they evolved - frequent fires and native megafaunal herbivory. In stark contrast, tropical grasslands are extremely vulnerable to human-caused exogenous disturbances, particularly those that alter soils and destroy belowground biomass (e.g. tillage agriculture, surface mining); tropical grassland restoration after severe soil disturbances is expensive and rarely achieves management targets. Where grasslands have been degraded by altered disturbance regimes (e.g. fire exclusion), exotic plant invasions, or afforestation, restoration efforts can recreate vegetation structure (i.e. historical tree density and herbaceous ground cover), but species-diverse plant communities, including endemic species, are slow to recover. Complicating plant-community restoration efforts, many tropical grassland species, particularly those that invest in underground storage organs, are difficult to propagate and re-establish. To guide restoration decisions, we draw on the old-growth grassland concept, the novel ecosystem concept, and theory regarding tree cover along resource gradients in savannas to propose a conceptual framework that classifies tropical grasslands into three broad ecosystem states. These states are: (1) old-growth grasslands (i.e. ancient, biodiverse grassy ecosystems), where management should focus on the maintenance of disturbance regimes; (2) hybrid grasslands, where restoration should emphasise a return towards the old-growth state; and (3) novel ecosystems, where the magnitude of environmental change (i.e. a shift to an alternative ecosystem state) or the socioecological context preclude a return to historical conditions.

Forest fragmentation in China and its effect on biodiversity.

Abstract: Land-use change is fragmenting natural ecosystems, with major consequences for biodiversity. This paper reviews fragmentation trends - historical and current - in China, the fourth largest country on Earth, and explores its consequences. Remote sensing makes it possible to track land-use change at a global scale and monitor fragmentation of dwindling natural landscapes. Yet few studies have linked fragmentation mapped remotely with impacts on biodiversity within human-modified landscapes. Recent reforestation programs have caused substantial increases in forest cover but have not stopped fragmentation, because the new forests are mostly monocultures that further fragment China's remnant old-growth lowland forests that harbour the highest levels of biodiversity. Fragmentation - and associated biodiversity declines - is unevenly distributed in China's forests, being most problematic where agricultural expansion is occurring in the southwest and northeast, serious in the densely populated eastern regions where urbanisation and transport infrastructure are modifying landscapes, but less of a problem in other regions. Analyses of temporal trends show that the drivers of forest fragmentation are shifting from mainly agricultural expansion to urbanisation and infrastructure development. Most of China's old-growth forests persist in small, isolated fragments from which many native species have disappeared, on land unsuitable for human utilisation. Fragmentation throughout China is likely to have major consequences on biodiversity conservation, but few studies have considered these large-scale processes at the national level. Our review fills this research gap and puts forward a systematic perspective relevant to China and beyond.

Mycorrhizal types differ in ecophysiology and alter plant nutrition and soil processes

Abstract: Mycorrhizal fungi benefit plants by improved mineral nutrition and protection against stress, yet information about fundamental differences among mycorrhizal types in fungi and trees and their relative importance in biogeochemical processes is only beginning to accumulate. We critically review and synthesize the ecophysiological differences in ectomycorrhizal, ericoid mycorrhizal and arbuscular mycorrhizal symbioses and the effect of these mycorrhizal types on soil processes from local to global scales. We demonstrate that guilds of mycorrhizal fungi display substantial differences in genome-encoded capacity for mineral nutrition, particularly acquisition of nitrogen and phosphorus from organic material. Mycorrhizal associations alter the trade-off between allocation to roots or mycelium, ecophysiological traits such as root exudation, weathering, enzyme production, plant protection, and community assembly as well as response to climate change. Mycorrhizal types exhibit differential effects on ecosystem carbon and nutrient cycling that affect global elemental fluxes and may mediate biome shifts in response to global change. We also note that most studies performed to date have not been properly replicated and collectively suffer from strong geographical sampling bias towards temperate biomes. We advocate that combining carefully replicated field experiments and controlled laboratory experiments with isotope labelling and -omics techniques offers great promise towards understanding differences in ecophysiology and ecosystem services among mycorrhizal types.

Fungal evolution: major ecological adaptations and evolutionary transitions.

Abstract: Fungi are a highly diverse group of heterotrophic eukaryotes characterized by the absence of phagotrophy and the presence of a chitinous cell wall. While unicellular fungi are far from rare, part of the evolutionary success of the group resides in their ability to grow indefinitely as a cylindrical multinucleated cell (hypha). Armed with these morphological traits and with an extremely high metabolical diversity, fungi have conquered numerous ecological niches and have shaped a whole world of interactions with other living organisms. Herein we survey the main evolutionary and ecological processes that have guided fungal diversity. We will first review the ecology and evolution of the zoosporic lineages and the process of terrestrialization, as one of the major evolutionary transitions in this kingdom. Several plausible scenarios have been proposed for fungal terrestralization and we here propose a new scenario, which considers icy environments as a transitory niche between water and emerged land. We then focus on exploring the main ecological relationships of Fungi with other organisms (other fungi, protozoans, animals and plants), as well as the origin of adaptations to certain specialized ecological niches within the group (lichens, black fungi and yeasts). Throughout this review we use an evolutionary and comparative-genomics perspective to understand fungal ecological diversity. Finally, we highlight the importance of genome-enabled inferences to envision plausible narratives and scenarios for important transitions.

Uncovering trophic positions and food resources of soil animals using bulk natural stable isotope composition.

Abstract: Despite the major importance of soil biota in nutrient and energy fluxes, interactions in soil food webs are poorly understood. Here we provide an overview of recent advances in uncovering the trophic structure of soil food webs using natural variations in stable isotope ratios. We discuss approaches of application, normalization and interpretation of stable isotope ratios along with methodological pitfalls. Analysis of published data from temperate forest ecosystems is used to outline emerging concepts and perspectives in soil food web research. In contrast to aboveground and aquatic food webs, trophic fractionation at the basal level of detrital food webs is large for carbon and small for nitrogen stable isotopes. Virtually all soil animals are enriched in 13 C as compared to plant litter. This 'detrital shift' likely reflects preferential uptake of 13 C-enriched microbial biomass and underlines the importance of microorganisms, in contrast to dead plant material, as a major food resource for the soil animal community. Soil organic matter is enriched in 15 N and 13 C relative to leaf litter. Decomposers inhabiting mineral soil layers therefore might be enriched in 15 N resulting in overlap in isotope ratios between soil-dwelling detritivores and litter-dwelling predators. By contrast, 13 C content varies little between detritivores in upper litter and in mineral soil, suggesting that they rely on similar basal resources, i.e. little decomposed organic matter. Comparing vertical isotope gradients in animals and in basal resources can be a valuable tool to assess trophic interactions and dynamics of organic matter in soil. As indicated by stable isotope composition, direct feeding on living plant material as well as on mycorrhizal fungi is likely rare among soil invertebrates. Plant carbon is taken up predominantly by saprotrophic microorganisms and channelled to higher trophic levels of the soil food web. However, feeding on photoautotrophic microorganisms and non-vascular plants may play an important role in fuelling soil food webs. The trophic niche of most high-rank animal taxa spans at least two trophic levels, implying the use of a wide range of resources. Therefore, to identify trophic species and links in food webs, low-rank taxonomic identification is required. Despite overlap in feeding strategies, stable isotope composition of the high-rank taxonomic groups reflects differences in trophic level and in the use of basal resources. Different taxonomic groups of predators and decomposers are likely linked to different pools of organic matter in soil, suggesting different functional roles and indicating that trophic niches in soil animal communities are phylogenetically structured. During last two decades studies using stable isotope analysis have elucidated the trophic structure of soil communities, clarified basal food resources of the soil food web and revealed links between above- and belowground ecosystem compartments. Extending the use of stable isotope analysis to a wider range of soil-dwelling organisms, including microfauna, and a larger array of ecosystems provides the perspective of a comprehensive understanding of the structure and functioning of soil food webs.

Synzoochory: the ecological and evolutionary relevance of a dual interaction.

Abstract: J.M.G. and P.J. were supported by CYTED program (Red Tematica 418RT0555). E.W.S. is supported by the Ecology Center and the Utah Agricultural Experiment Station (UAES), Utah State University. P.J. is supported by grant CGL2017‐82847‐P from the Spanish Ministry of Science, Innovation, and Universities (AEI).

Sexual selection and its evolutionary consequences in female animals.

Abstract: For sexual selection to act on a given sex, there must exist variation in the reproductive success of that sex as a result of differential access to mates or fertilisations. The mechanisms and consequences of sexual selection acting on male animals are well documented, but research on sexual selection acting on females has only recently received attention. Controversy still exists over whether sexual selection acts on females in the traditional sense, and over whether to modify the existing definition of sexual selection (to include resource competition) or to invoke alternative mechanisms (usually social selection) to explain selection acting on females in connection with reproduction. However, substantial evidence exists of females bearing characters or exhibiting behaviours that result in differential reproductive success that are analogous to those attributed to sexual selection in males. Here we summarise the literature and provide substantial evidence of female intrasexual competition for access to mates, female intersexual signalling to potential mates, and postcopulatory mechanisms such as competition between eggs for access to sperm and cryptic male allocation. Our review makes clear that sexual selection acts on females and males in similar ways but sometimes to differing extents: the ceiling for the elaboration of costly traits may be lower in females than in males. We predict that current and future research on female sexual selection will provide increasing support for the parsimony and utility of the existing definition of sexual selection.

Intrasexually selected weapons.

Abstract: We propose a practical concept that distinguishes the particular kind of weaponry that has evolved to be used in combat between individuals of the same species and sex, which we term intrasexually selected weapons (ISWs). We present a treatise of ISWs in nature, aiming to understand their distinction and evolution from other secondary sex traits, including from 'sexually selected weapons', and from sexually dimorphic and monomorphic weaponry. We focus on the subset of secondary sex traits that are the result of same-sex combat, defined here as ISWs, provide not previously reported evolutionary patterns, and offer hypotheses to answer questions such as: why have only some species evolved weapons to fight for the opposite sex or breeding resources? We examined traits that seem to have evolved as ISWs in the entire animal phylogeny, restricting the classification of ISW to traits that are only present or enlarged in adults of one of the sexes, and are used as weapons during intrasexual fights. Because of the absence of behavioural data and, in many cases, lack of sexually discriminated series from juveniles to adults, we exclude the fossil record from this review. We merge morphological, ontogenetic, and behavioural information, and for the first time thoroughly review the tree of life to identify separate evolution of ISWs. We found that ISWs are only found in bilateral animals, appearing independently in nematodes, various groups of arthropods, and vertebrates. Our review sets a reference point to explore other taxa that we identify with potential ISWs for which behavioural or morphological studies are warranted. We establish that most ISWs come in pairs, are located in or near the head, are endo- or exoskeletal modifications, are overdeveloped structures compared with those found in females, are modified feeding structures and/or locomotor appendages, are most common in terrestrial taxa, are frequently used to guard females, territories, or both, and are also used in signalling displays to deter rivals and/or attract females. We also found that most taxa lack ISWs, that females of only a few species possess better-developed weapons than males, that the cases of independent evolution of ISWs are not evenly distributed across the phylogeny, and that animals possessing the most developed ISWs have non-hunting habits (e.g. herbivores) or are faunivores that prey on very small prey relative to their body size (e.g. insectivores). Bringing together perspectives from studies on a variety of taxa, we conceptualize that there are five ways in which a sexually dimorphic trait, apart from the primary sex traits, can be fixed: sexual selection, fecundity selection, parental role division, differential niche occupation between the sexes, and interference competition. We discuss these trends and the factors involved in the evolution of intrasexually selected weaponry in nature.

Diversity in warning coloration: selective paradox or the norm?

Abstract: Aposematic theory has historically predicted that predators should select for warning signals to converge on a single form, as a result of frequency-dependent learning However, widespread variation in warning signals is observed across closely related species, populations and, most problematically for evolutionary biologists, among individuals in the same population Recent research has yielded an increased awareness of this diversity, challenging the paradigm of signal monomorphy in aposematic animals Here we provide a comprehensive synthesis of these disparate lines of investigation, identifying within them three broad classes of explanation for variation in aposematic warning signals: genetic mechanisms, differences among predators and predator behaviour, and alternative selection pressures upon the signal The mechanisms producing warning coloration are also important Detailed studies of the genetic basis of warning signals in some species, most notably Heliconius butterflies, are beginning to shed light on the genetic architecture facilitating or limiting key processes such as the evolution and maintenance of polymorphisms, hybridisation, and speciation Work on predator behaviour is changing our perception of the predator community as a single homogenous selective agent, emphasising the dynamic nature of predator-prey interactions Predator variability in a range of factors (eg perceptual abilities, tolerance to chemical defences, and individual motivation), suggests that the role of predators is more complicated than previously appreciated With complex selection regimes at work, polytypisms and polymorphisms may even occur in Mullerian mimicry systems Meanwhile, phenotypes are often multifunctional, and thus subject to additional biotic and abiotic selection pressures Some of these selective pressures, primarily sexual selection and thermoregulation, have received considerable attention, while others, such as disease risk and parental effects, offer promising avenues to explore As well as reviewing the existing evidence from both empirical studies and theoretical modelling, we highlight hypotheses that could benefit from further investigation in aposematic species Finally by collating known instances of variation in warning signals, we provide a valuable resource for understanding the taxonomic spread of diversity in aposematic signalling and with which to direct future research A greater appreciation of the extent of variation in aposematic species, and of the selective pressures and constraints which contribute to this once-paradoxical phenomenon, yields a new perspective for the field of aposematic signalling

Causes and consequences of ontogenetic dietary shifts: a global synthesis using fish models

Abstract: Ontogenetic dietary shifts (ODSs), the changes in diet utilisation occurring over the life span of an individual consumer, are widespread in the animal kingdom. Understanding ODSs provides fundamental insights into the biological and ecological processes that function at the individual, population and community levels, and is critical for the development and testing of hypotheses around key concepts in trophic theory on model organisms. Here, we synthesise historic and contemporary research on ODSs in fishes, and identify where further research is required. Numerous biotic and abiotic factors can directly or indirectly influence ODSs, but the most influential of these may vary spatially, temporally and interspecifically. Within the constraints imposed by prey availability, we identified competition and predation risk as the major drivers of ODSs in fishes. These drivers do not directly affect the trophic ontogeny of fishes, but may have an indirect effect on diet trajectories through ontogenetic changes in habitat use and concomitant changes in prey availability. The synthesis provides compelling evidence that ODSs can have profound ecological consequences for fish by, for example, enhancing individual growth and lifetime reproductive output or reducing the risk of mortality. ODSs may also influence food‐web dynamics and facilitate the coexistence of sympatric species through resource partitioning, but we currently lack a holistic understanding of the consequences of ODSs for population, community and ecosystem processes and functioning. Studies attempting to address these knowledge gaps have largely focused on theoretical approaches, but empirical research under natural conditions, including phylogenetic and evolutionary considerations, is required to test the concepts. Research focusing on inter‐individual variation in ontogenetic trajectories has also been limited, with the complex relationships between individual behaviour and environmental heterogeneity representing a particularly promising area for future research.

A review of Gloger's rule, an ecogeographical rule of colour: definitions, interpretations and evidence.

Abstract: Gloger's rule is an ecogeographical rule that links animal colouration with climatic variation. This rule is named after C.W.L. Gloger who was one of the first to summarise the associations between climatic variation and animal colouration, noting in particular that birds and mammals seemed more pigmented in tropical regions. The term 'Gloger's rule' was coined by B. Rensch in 1929 and included different patterns of variation from those described by Gloger. Rensch defined the rule in two ways: a simple version stating that endothermic animals are predicted to be darker in warmer and humid areas due to the increased deposition of melanin pigments; and a complex version that includes the differential effects of humidity and temperature on both main types of melanin pigments - eu- and phaeo-melanin. The blackish eu-melanins are predicted to increase with humidity, and decrease only at extreme low temperatures, while the brown-yellowish phaeomelanins prevail in dry and warm regions and decrease rapidly with lower temperatures. A survey of the literature indicates that there is considerable variation/confusion in the way Gloger's rule is understood (based on 271 studies that define the rule). Whereas the complex version is hardly mentioned, only a quarter of the definitions are consistent with the simple version of Gloger's rule (darker where warm and wet), and most definitions mention only the effects of humidity (darker where wet). A smaller subset of studies define the rule based on other correlated climatic and environmental variables such as vegetation, latitude, altitude, solar radiation, etc., and a few even contradict the original definition (darker where cold). Based on the literature survey, I synthesised the qualitative (N = 124 studies) and quantitative (meta-analytically, N = 38 studies, 241 effects) evidence testing the simple version of Gloger's rule (I found no tests of the complex version). Both lines of evidence supported the predicted effects of humidity (and closely linked variables) on colour variation, but not the effects of temperature. Moreover, humidity effects are not restricted to birds and mammals, as the data indicate that these effects also apply to insects. This suggests that the simple version of Gloger's rule as originally defined may not be valid, and possibly that the rule should be re-formulated in terms of humidity effects only. I suggest, however, that more data are needed before such a reformulation, due to potential publication biases. In conclusion, I recommend that authors cite Rensch when referring to Gloger's rule and that they make clear which version they are referring to. Future research should concentrate on rigorously testing the validity and generality of both versions of Gloger's rule and establishing the mechanism(s) responsible for the patterns it describes. Since humidity seems to be the core climatic variable behind Gloger's rule, I suggest that the two most plausible mechanisms are camouflage and protection against parasites/pathogens, the latter possibly through pleiotropic effects on the immune system. Understanding the processes that lead to climatic effects on animal colouration may provide insights into past and future patterns of adaptation to climatic change.

Life-history evolution under fluctuating density-dependent selection and the adaptive alignment of pace-of-life syndromes.

Abstract: We present a novel perspective on life-history evolution that combines recent theoretical advances in fluctuating density-dependent selection with the notion of pace-of-life syndromes (POLSs) in behavioural ecology These ideas posit phenotypic co-variation in life-history, physiological, morphological and behavioural traits as a continuum from the highly fecund, short-lived, bold, aggressive and highly dispersive 'fast' types at one end of the POLS to the less fecund, long-lived, cautious, shy, plastic and socially responsive 'slow' types at the other We propose that such variation in life histories and the associated individual differences in behaviour can be explained through their eco-evolutionary dynamics with population density - a single and ubiquitous selective factor that is present in all biological systems Contrasting regimes of environmental stochasticity are expected to affect population density in time and space and create differing patterns of fluctuating density-dependent selection, which generates variation in fast versus slow life histories within and among populations We therefore predict that a major axis of phenotypic co-variation in life-history, physiological, morphological and behavioural traits (ie the POLS) should align with these stochastic fluctuations in the multivariate fitness landscape created by variation in density-dependent selection Phenotypic plasticity and/or genetic (co-)variation oriented along this major POLS axis are thus expected to facilitate rapid and adaptively integrated changes in various aspects of life histories within and among populations and/or species The fluctuating density-dependent selection POLS framework presented here therefore provides a series of clear testable predictions, the investigation of which should further our fundamental understanding of life-history evolution and thus our ability to predict natural population dynamics

Animal movements in fire-prone landscapes

Abstract: Movement is a trait of fundamental importance in ecosystems subject to frequent disturbances, such as fire-prone ecosystems. Despite this, the role of movement in facilitating responses to fire has received little attention. Herein, we consider how animal movement interacts with fire history to shape species distributions. We consider how fire affects movement between habitat patches of differing fire histories that occur across a range of spatial and temporal scales, from daily foraging bouts to infrequent dispersal events, and annual migrations. We review animal movements in response to the immediate and abrupt impacts of fire, and the longer-term successional changes that fires set in train. We discuss how the novel threats of altered fire regimes, landscape fragmentation, and invasive species result in suboptimal movements that drive populations downwards. We then outline the types of data needed to study animal movements in relation to fire and novel threats, to hasten the integration of movement ecology and fire ecology. We conclude by outlining a research agenda for the integration of movement ecology and fire ecology by identifying key research questions that emerge from our synthesis of animal movements in fire-prone ecosystems.

Adaptive evolution of butterfly wing shape: from morphology to behaviour

Abstract: Butterflies display extreme variation in wing shape associated with tremendous ecological diversity. Disentangling the role of neutral versus adaptive processes in wing shape diversification remains a challenge for evolutionary biologists. Ascertaining how natural selection influences wing shape evolution requires both functional studies linking morphology to flight performance, and ecological investigations linking performance in the wild with fitness. However, direct links between morphological variation and fitness have rarely been established. The functional morphology of butterfly flight has been investigated but selective forces acting on flight behaviour and associated wing shape have received less attention. Here, we attempt to estimate the ecological relevance of morpho-functional links established through biomechanical studies in order to understand the evolution of butterfly wing morphology. We survey the evidence for natural and sexual selection driving wing shape evolution in butterflies, and discuss how our functional knowledge may allow identification of the selective forces involved, at both the macro- and micro-evolutionary scales. Our review shows that although correlations between wing shape variation and ecological factors have been established at the macro-evolutionary level, the underlying selective pressures often remain unclear. We identify the need to investigate flight behaviour in relevant ecological contexts to detect variation in fitness-related traits. Identifying the selective regime then should guide experimental studies towards the relevant estimates of flight performance. Habitat, predators and sex-specific behaviours are likely to be major selective forces acting on wing shape evolution in butterflies. Some striking cases of morphological divergence driven by contrasting ecology involve both wing and body morphology, indicating that their interactions should be included in future studies investigating co-evolution between morphology and flight behaviour.

A way forward with eco evo devo: an extended theory of resource polymorphism with postglacial fishes as model systems

Abstract: A major goal of evolutionary science is to understand how biological diversity is generated and altered. Despite considerable advances, we still have limited insight into how phenotypic variation a ...

A general framework for propagule dispersal in mangroves.

Abstract: Dispersal allows species to shift their distributions in response to changing climate conditions. As a result, dispersal is considered a key process contributing to a species' long-term persistence. For many passive dispersers, fluid dynamics of wind and water fuel these movements and different species have developed remarkable adaptations for utilizing this energy to reach and colonize suitable habitats. The seafaring propagules (fruits and seeds) of mangroves represent an excellent example of such passive dispersal. Mangroves are halophytic woody plants that grow in the intertidal zones along tropical and subtropical shorelines and produce hydrochorous propagules with high dispersal potential. This results in exceptionally large coastal ranges across vast expanses of ocean and allows species to shift geographically and track the conditions to which they are adapted. This is particularly relevant given the challenges presented by rapid sea-level rise, higher frequency and intensity of storms, and changes in regional precipitation and temperature regimes. However, despite its importance, the underlying drivers of mangrove dispersal have typically been studied in isolation, and a conceptual synthesis of mangrove oceanic dispersal across spatial scales is lacking. Here, we review current knowledge on mangrove propagule dispersal across the various stages of the dispersal process. Using a general framework, we outline the mechanisms and ecological processes that are known to modulate the spatial patterns of mangrove dispersal. We show that important dispersal factors remain understudied and that adequate empirical data on the determinants of dispersal are missing for most mangrove species. This review particularly aims to provide a baseline for developing future research agendas and field campaigns, filling current knowledge gaps and increasing our understanding of the processes that shape global mangrove distributions.

The covariance between metabolic rate and behaviour varies across behaviours and thermal types: meta-analytic insights

Abstract: Energy metabolism has received much attention as a potential driver of repeatable among-individual differences in behaviour (animal personality). Several factors have been hypothesized to mediate this relationship. We performed a systematic review with a meta-analysis of >70 studies comprised of >8000 individuals reporting relationships between measures of maintenance metabolic rates (i.e. basal metabolic rate, resting metabolic rate, and standard metabolic rate) and behaviour. We evaluated support for three hypothesized mediators: (i) type of behaviour, (ii) opportunities for energy re-allocation, and (iii) magnitude of energetic constraints. Relationships between measures of maintenance metabolic rate (MR) and behaviour are predicted to be strongest for behaviours with strong consequences for energy turnover (acquisition or expenditure). Consistent with this, we found that behaviours with known consequences for energy gain (e.g. foraging, dominance, boldness) or expenditure (e.g. maximum sprint speed, sustained running speed, maximum distance travelled, etc.) had strong positive correlations with MR, while behaviours with putatively weak and/or inconsistent associations with net energy gain or loss (e.g. exploration, activity, sociability) were not correlated with MR. Greater opportunities for energy reallocation are predicted to weaken relationships between MR and behaviour by creating alternative pathways to balance energy budgets. We tested this by contrasting relationships between MR and behaviour in ectotherms versus endotherms, as thermoregulation in endotherms creates additional opportunities for energy reallocation compared with ectotherms. As predicted, the relationship between behaviour and MR was stronger in ectotherms compared with endotherms. However, statistical analyses of heterogeneity among effect sizes from different species did not support energy re-allocation as the main driver of these differences. Finally, we tested whether conditions where animals face greater constraints in meeting their energy budgets (e.g. field versus laboratory, breeding versus non-breeding) increased the strength of the relationship between MR and behaviour. We found that the relationship between MR and behaviour was unaffected by either of these modifiers. This meta-analysis provides two key insights. First, we observed positive relationships of similar magnitude between MR and behaviours that bring in net energy, and behaviours that cost net energy. This result is only consistent with a performance energy-management model. Given that the studies included in our meta-analysis represent a wide range of taxa, this suggests that the performance model may be the most common model in general. Second, we found that behaviours with putatively weak or inconsistent consequences for net energy gain or expenditure (exploration, activity, sociability) show no relationship with MR. The lack of relationship between MR and behavioural traits with weak and/or inconsistent consequences for energy turnover provides the first systematic demonstration of the central importance of the ecological function of traits in mediating relationships between MR and behaviour.

Evolutionary history of fire-stimulated resprouting, flowering, seed release and germination.

Abstract: Fire has shaped the evolution of many plant traits in fire-prone environments: fire-resistant tissues with heat-insulated meristems, post-fire resprouting or fire-killed but regenerating from stored seeds, fire-stimulated flowering, release of on-plant-stored seeds, and germination of soil-stored seeds. Flowering, seed release and germination fit into three categories of response to intensifying fire: fire not required, weakly fire-adapted or strongly fire-adapted. Resprouting also has three categories but survival is always reduced by increasing fire intensity. We collated 286 records for 20 angiosperm and two gymnosperm families and 50 trait assignments to dated phylogenies. We placed these into three fire-adapted trait types: those associated with the origin of their clade and the onset of fire-proneness [primary diversification, contributing 20% of speciation events over the last 120 million years (My)], those originating much later coincident with a change in the fire regime (secondary diversification, 30%), and those conserved in the daughter lineage as already adapted to the fire regime (stabilisation, 50%). All four fire-response types could be traced to >100 My ago (Mya) with pyrogenic flowering slightly younger because of its dependence on resprouting. There was no evidence that resprouting was always an older trait than either seed storage or non-sprouting throughout this period, with either/both ancestral or derived in different clades and times. Fire-adapted traits evolved slowly in the Cretaceous, 120-65 Mya, and rapidly but fitfully in the Cenozoic, 65-0 Mya, peaking over the last 20 My. The four trait-types climaxed at different times, with the peak in resprouter speciation over the last 5 My attributable to fluctuating growing conditions and increasing savanna grasslands unsuitable for non-sprouters. All experienced a trough in the 40-30-Mya period following a reduction in world temperatures and oxygen levels and expected reduced fire activity. Thick bark and serotiny arose in the Mid-Cretaceous among extant Pinaceae. Heat-stimulated germination of hard seeds is ancestral in the 103-My-old Fabales. Smoke-(karrikin)-stimulated germination of non-hard seeds is even older, and includes the 101-My-old Restionaceae-Anarthriaceae. A smoke/karrikin response is detectable in some fire-free lineages that prove to have a fire-prone ancestry. Among clades that are predominantly fire-prone, absence of fire-related traits is the advanced condition, associated either with increased fire frequency (loss of serotiny and soil storage), or migration to fire-free habitats (loss of thick bark, pyrogenic flowering, serotiny or soil storage). Protea (Africa) and Hakea (Australia) illustrate the importance of stabilisation processes between resprouting/non-sprouting in accounting for speciation events over the last 20 My and highlight the frequent interchange possible between these two traits. Apart from Pinus, most ancestral trait reconstruction relative to fire has been conducted on predominantly Southern Hemisphere clades and this needs to be redressed. Despite these limitations, it is clear that fire has had a profound effect on fire-related trait evolution worldwide, and set the platform for subsequent evolution of many non-fire-related traits. Genetics of the triggering mechanisms remain poorly understood, except the karrikin system for smoke-stimulated germination. We exhort biologists to include fire-proneness and fire-related traits in their thinking on possible factors controlling the evolution of plants.

Epigenetically facilitated mutational assimilation: epigenetics as a hub within the inclusive evolutionary synthesis

Abstract: After decades of debate about the existence of non‐genetic inheritance, the focus is now slowly shifting towards dissecting its underlying mechanisms. Here, we propose a new mechanism that, by integrating non‐genetic and genetic inheritance, may help build the long‐sought inclusive vision of evolution. After briefly reviewing the wealth of evidence documenting the existence and ubiquity of non‐genetic inheritance in a table, we review the categories of mechanisms of parent–offspring resemblance that underlie inheritance. We then review several lines of argument for the existence of interactions between non‐genetic and genetic components of inheritance, leading to a discussion of the contrasting timescales of action of non‐genetic and genetic inheritance. This raises the question of how the fidelity of the inheritance system can match the rate of environmental variation. This question is central to understanding the role of different inheritance systems in evolution. We then review and interpret evidence indicating the existence of shifts from inheritance systems with low to higher transmission fidelity. Based on results from different research fields we propose a conceptual hypothesis linking genetic and non‐genetic inheritance systems. According to this hypothesis, over the course of generations, shifts among information systems allow gradual matching between the rate of environmental change and the inheritance fidelity of the corresponding response. A striking conclusion from our review is that documented shifts between types of inherited non‐genetic information converge towards epigenetics (i.e. inclusively heritable molecular variation in gene expression without change in DNA sequence). We then interpret the well‐documented mutagenicity of epigenetic marks as potentially generating a final shift from epigenetic to genetic encoding. This sequence of shifts suggests the existence of a relay in inheritance systems from relatively labile ones to gradually more persistent modes of inheritance, a relay that could constitute a new mechanistic basis for the long‐proposed, but still poorly documented, hypothesis of genetic assimilation. A profound difference between the genocentric and the inclusive vision of heredity revealed by the genetic assimilation relay proposed here lies in the fact that a given form of inheritance can affect the rate of change of other inheritance systems. To explore the consequences of such inter‐connection among inheritance systems, we briefly review published theoretical models to build a model of genetic assimilation focusing on the shift in the engraving of environmentally induced phenotypic variation into the DNA sequence. According to this hypothesis, when environmental change remains stable over a sufficient number of generations, the relay among inheritance systems has the potential to generate a form of genetic assimilation. In this hypothesis, epigenetics appears as a hub by which non‐genetically inherited environmentally induced variation in traits can become genetically encoded over generations, in a form of epigenetically facilitated mutational assimilation. Finally, we illustrate some of the major implications of our hypothetical framework, concerning mutation randomness, the central dogma of molecular biology, concepts of inheritance and the curing of inherited disorders, as well as for the emergence of the inclusive evolutionary synthesis.

Ommochromes in invertebrates: biochemistry and cell biology.

Abstract: Ommochromes are widely occurring coloured molecules of invertebrates, arising from tryptophan catabolism through the so-called Tryptophan → Ommochrome pathway. They are mainly known to mediate compound eye vision, as well as reversible and irreversible colour patterning. Ommochromes might also be involved in cell homeostasis by detoxifying free tryptophan and buffering oxidative stress. These biological functions are directly linked to their unique chromophore, the phenoxazine/phenothiazine system. The most recent reviews on ommochrome biochemistry were published more than 30 years ago, since when new results on the enzymes of the ommochrome pathway, on ommochrome photochemistry as well as on their antiradical capacities have been obtained. Ommochromasomes are the organelles where ommochromes are synthesised and stored. Hence, they play an important role in mediating ommochrome functions. Ommochromasomes are part of the lysosome-related organelles (LROs) family, which includes other pigmented organelles such as vertebrate melanosomes. Ommochromasomes are unique because they are the only LRO for which a recycling process during reversible colour change has been described. Herein, we provide an update on ommochrome biochemistry, photoreactivity and antiradical capacities to explain their diversity and behaviour both in vivo and in vitro. We also highlight new biochemical techniques, such as quantum chemistry, metabolomics and crystallography, which could lead to major advances in their chemical and functional characterisation. We then focus on ommochromasome structure and formation by drawing parallels with the well-characterised melanosomes of vertebrates. The biochemical, genetic, cellular and microscopic tools that have been applied to melanosomes should provide important information on the ommochromasome life cycle. We propose LRO-based models for ommochromasome biogenesis and recycling that could be tested in the future. Using the context of insect compound eyes, we finally emphasise the importance of an integrated approach in understanding the biological functions of ommochromes.

What, where and when: spatial foraging decisions in primates.

Abstract: When exploiting the environment, animals have to discriminate, track, and integrate salient spatial cues to navigate and identify goal sites Actually, they have to know what can be found (eg what fruit), where (eg on which tree) and when (in what season or moment of the year) This is very relevant for primate species as they often live in seasonal and relatively unpredictable environments such as tropical forests Here, we review and compare different approaches used to investigate primate spatial foraging strategies: from direct observations of wild primates to predictions from statistical simulations, including experimental approaches on both captive and wild primates, and experiments in captivity using virtual reality technology Within this framework, most of these studies converge to show that many primate species can (i) remember the location of most of food resources well, and (ii) often seem to have a goal-oriented path towards spatially permanent resources Overall, primates likely use mental maps to plan different foraging strategies to enhance their fitness The majority of studies suggest that they may organise spatial information on food resources into topological maps: they use landmarks to navigate and encode local spatial information with regard to direction and distance Even though these studies were able to show that primates can remember food quality (what) and its location (where), still very little is known on how they incorporate the temporal knowledge of available food (when) Future studies should attempt to increase our understanding of the potential of primates to learn temporal patterns and how both socio-ecological differences among species and their cognitive abilities influence such behavioural strategies

Death among primates: a critical review of non-human primate interactions towards their dead and dying.

Abstract: For the past two centuries, non-human primates have been reported to inspect, protect, retrieve, carry or drag the dead bodies of their conspecifics and, for nearly the same amount of time, sparse scientific attention has been paid to such behaviours. Given that there exists a considerable gap in the fossil and archaeological record concerning how early hominins might have interacted with their dead, extant primates may provide valuable insight into how and in which contexts thanatological behaviours would have occurred. First, we outline a comprehensive history of comparative thanatology in non-human primates, from the earliest accounts to the present, uncovering the interpretations of previous researchers and their contributions to the field of primate thanatology. Many of the typical behavioural patterns towards the dead seen in the past are consistent with those observed today. Second, we review recent evidence of thanatological responses and organise it into distinct terminologies: direct interactions (physical contact with the corpse) and secondary interactions (guarding the corpse, vigils and visitations). Third, we provide a critical evaluation regarding the form and function of the behavioural and emotional aspects of these responses towards infants and adults, also comparing them with non-conspecifics. We suggest that thanatological interactions: promote a faster re-categorisation from living to dead, decrease costly vigilant/caregiving behaviours, are crucial to the management of grieving responses, update position in the group's hierarchy, and accelerate the formation of new social bonds. Fourth, we propose an integrated model of Life-Death Awareness, whereupon neural circuitry dedicated towards detecting life, i.e. the agency system (animate agency, intentional agency, mentalistic agency) works with a corresponding system that interacts with it on a decision-making level (animate/inanimate distinction, living/dead discrimination, death awareness). Theoretically, both systems are governed by specific cognitive mechanisms (perceptual categories, associative concepts and high-order reasoning, respectively). Fifth, we present an evolutionary timeline from rudimentary thanatological responses likely occurring in earlier non-human primates during the Eocene to the more elaborate mortuary practices attributed to genus Homo throughout the Pleistocene. Finally, we discuss the importance of detailed reports on primate thanatology and propose several empirical avenues to shed further light on this topic. This review expands and builds upon previous attempts to evaluate the body of knowledge on this subject, providing an integrative perspective and bringing together different fields of research to detail the evolutionary, sensory/cognitive, developmental and historical/archaeological aspects of primate thanatology. Considering all these findings and given their cognitive abilities, we argue that non-human primates are capable of an implicit awareness of death.

The physiological roles of autophagy in the mammalian life cycle.

Abstract: Autophagy is primarily an efficient intracellular catabolic pathway used for degradation of abnormal cellular protein aggregates and damaged organelles. Although autophagy was initially proposed to be a cellular stress responder, increasing evidence suggests that it carries out normal physiological roles in multiple biological processes. To date, autophagy has been identified in most organs and at many different developmental stages, indicating that it is not only essential for cellular homeostasis and renovation, but is also important for organ development. Herein, we summarize our current understanding of the functions of autophagy (which here refers to macroautophagy) in the mammalian life cycle.

Laminins and their receptors in the CNS.

Abstract: Laminin, an extracellular matrix protein, is widely expressed in the central nervous system (CNS). By interacting with integrin and non-integrin receptors, laminin exerts a large variety of important functions in the CNS in both physiological and pathological conditions. Due to the existence of many laminin isoforms and their differential expression in various cell types in the CNS, the exact functions of each individual laminin molecule in CNS development and homeostasis remain largely unclear. In this review, we first briefly introduce the structure and biochemistry of laminins and their receptors. Next, the dynamic expression of laminins and their receptors in the CNS during both development and in adulthood is summarized in a cell-type-specific manner, which allows appreciation of their functional redundancy/compensation. Furthermore, we discuss the biological functions of laminins and their receptors in CNS development, blood-brain barrier (BBB) maintenance, neurodegeneration, stroke, and neuroinflammation. Last, key challenges and potential future research directions are summarized and discussed. Our goals are to provide a synthetic review to stimulate future studies and promote the formation of new ideas/hypotheses and new lines of research in this field.

Multimodal communication and language origins: integrating gestures and vocalizations.

Abstract: The presence of divergent and independent research traditions in the gestural and vocal domains of primate communication has resulted in major discrepancies in the definition and operationalization of cognitive concepts. However, in recent years, accumulating evidence from behavioural and neurobiological research has shown that both human and non‐human primate communication is inherently multimodal. It is therefore timely to integrate the study of gestural and vocal communication. Herein, we review evidence demonstrating that there is no clear difference between primate gestures and vocalizations in the extent to which they show evidence for the presence of key language properties: intentionality, reference, iconicity and turn‐taking. We also find high overlap in the neurobiological mechanisms producing primate gestures and vocalizations, as well as in ontogenetic flexibility. These findings confirm that human language had multimodal origins. Nonetheless, we note that in great apes, gestures seem to fulfil a carrying (i.e. predominantly informative) role in close‐range communication, whereas the opposite holds for face‐to‐face interactions of humans. This suggests an evolutionary shift in the carrying role from the gestural to the vocal stream, and we explore this transition in the carrying modality. Finally, we suggest that future studies should focus on the links between complex communication, sociality and cooperative tendency to strengthen the study of language origins.

Effects of developmental stress on animal phenotype and performance: a quantitative review

Abstract: Developmental stressors are increasingly recognised for their pervasive influence on the ecology and evolution of animals. In particular, many studies have focused on how developmental stress can give rise to variation in adult behaviour, physiology, and performance. However, there remains a poor understanding of whether general patterns exist in the effects and magnitude of phenotypic responses across taxonomic groups. Furthermore, given the extensive phenotypic variation that arises from developmental stressors, it remains important to ascertain how multiple processes may explain these responses. We compiled data from 111 studies to examine and quantify the effect of developmental stress on animal phenotype and performance from juveniles to adulthood, including studies from birds, reptiles, fish, mammals, insects, arachnids, and amphibians. Using meta-analytic approaches, we show that across all studies there is, on average, a moderate to large negative effect of developmental stress exposure (posterior mean effect: |d| = -0.51) on animal phenotype or performance. Additionally, we demonstrate that interactive effects of timing of stressor onset and the duration of exposure to stressors best explained variation in developmental stress responses. Animals exposed to stressors earlier in development had more-positive responses than those with later onset, whereas longer duration of exposure to a stressor caused responses to be stronger in magnitude. However, the high amount of heterogeneity in our results, and the low degree of variance explained by fixed effects in both the meta-analysis (R2 = 0.034) and top-ranked meta-regression model (R2 = 0.02), indicate that phenotypic responses to developmental stressors are likely highly idiosyncratic in nature and difficult to predict. Despite this, our analyses address a critical knowledge gap in understanding what effect developmental stress has on phenotypic variation in animals. Additionally, our results highlight important environmental and proximate factors that may influence phenotypic responses to developmental stressors.

Reintroduction of freshwater macroinvertebrates: challenges and opportunities.

Abstract: Species reintroductions – the translocation of individuals to areas in which a species has been extirpated with the aim of re-establishing a self-sustaining population – have become a widespread practice in conservation biology. Reintroduction projects have tended to focus on terrestrial vertebrates and, to a lesser extent, fishes. Much less effort has been devoted to the reintroduction of invertebrates into restored freshwater habitats. Yet, reintroductions may improve restoration outcomes in regions where impoverished regional species pools limit the self-recolonisation of restored freshwaters. We review the available literature on macroinvertebrate reintroductions, focusing on identifying the intrinsic and extrinsic factors that determine their success or failure. Our study reveals that freshwater macroinvertebrate reintroductions remain rare, are often published in the grey literature and, of the attempts made, approximately one-third fail. We identify life-cycle complexity and remaining stressors as the two factors most likely to affect reintroduction success, illustrating the unique challenges of freshwater macroinvertebrate reintroductions. Consideration of these factors by managers during the planning process and proper documentation – even if a project fails – may increase the likelihood of successful outcomes in future reintroduction attempts of freshwater macroinvertebrates.

Using the Value of Information to improve conservation decision making.

Abstract: Conservation decisions are challenging, not only because they often involve difficult conflicts among outcomes that people value, but because our understanding of the natural world and our effects on it is fraught with uncertainty. Value of Information (VoI) methods provide an approach for understanding and managing uncertainty from the standpoint of the decision maker. These methods are commonly used in other fields (e.g. economics, public health) and are increasingly used in biodiversity conservation. This decision-analytical approach can identify the best management alternative to select where the effectiveness of interventions is uncertain, and can help to decide when to act and when to delay action until after further research. We review the use of VoI in the environmental domain, reflect on the need for greater uptake of VoI, particularly for strategic conservation planning, and suggest promising areas for new research. We also suggest common reporting standards as a means of increasing the leverage of this powerful tool. The environmental science, ecology and biodiversity categories of the Web of Knowledge were searched using the terms 'Value of Information,' 'Expected Value of Perfect Information,' and the abbreviation 'EVPI.' Google Scholar was searched with the same terms, and additionally the terms decision and biology, biodiversity conservation, fish, or ecology. We identified 1225 papers from these searches. Included studies were limited to those that showed an application of VoI in biodiversity conservation rather than simply describing the method. All examples of use of VOI were summarised regarding the application of VoI, the management objectives, the uncertainties, the models used, how the objectives were measured, and the type of VoI. While the use of VoI appears to be on the increase in biodiversity conservation, the reporting of results is highly variable, which can make it difficult to understand the decision context and which uncertainties were considered. Moreover, it was unclear if, and how, the papers informed management and policy interventions, which is why we suggest a range of reporting standards that would aid the use of VoI. The use of VoI in conservation settings is at an early stage. There are opportunities for broader applications, not only for species-focussed management problems, but also for setting local or global research priorities for biodiversity conservation, making funding decisions, or designing or improving protected area networks and management. The long-term benefits of applying VoI methods to biodiversity conservation include a more structured and decision-focused allocation of resources to research.