Showing papers in "Biological Reviews in 2021"

Tectonics, climate and the diversification of the tropical African terrestrial flora and fauna

Abstract: Tropical Africa is home to an astonishing biodiversity occurring in a variety of ecosystems. Past climatic change and geological events have impacted the evolution and diversification of this biodiversity. During the last two decades, around 90 dated molecular phylogenies of different clades across animals and plants have been published leading to an increased understanding of the diversification and speciation processes generating tropical African biodiversity. In parallel, extended geological and palaeoclimatic records together with detailed numerical simulations have refined our understanding of past geological and climatic changes in Africa. To date, these important advances have not been reviewed within a common framework. Here, we critically review and synthesize African climate, tectonics and terrestrial biodiversity evolution throughout the Cenozoic to the mid-Pleistocene, drawing on recent advances in Earth and life sciences. We first review six major geo-climatic periods defining tropical African biodiversity diversification by synthesizing 89 dated molecular phylogeny studies. Two major geo-climatic factors impacting the diversification of the sub-Saharan biota are highlighted. First, Africa underwent numerous climatic fluctuations at ancient and more recent timescales, with tectonic, greenhouse gas, and orbital forcing stimulating diversification. Second, increased aridification since the Late Eocene led to important extinction events, but also provided unique diversification opportunities shaping the current tropical African biodiversity landscape. We then review diversification studies of tropical terrestrial animal and plant clades and discuss three major models of speciation: (i) geographic speciation via vicariance (allopatry); (ii) ecological spe-ciation impacted by climate and geological changes, and (iii) genomic speciation via genome duplication. Geographic speciation has been the most widely documented to date and is a common speciation model across tropical Africa. We conclude with four important challenges faced by tropical African biodiversity research: (i) to increase knowledge by gathering basic and fundamental biodiversity information; (ii) to improve modelling of African geophysical evolution throughout the Cenozoic via better constraints and downscaling approaches; (iii) to increase the precision of phylogenetic reconstruction and molecular dating of tropical African clades by using next generation sequencing approaches together with better fossil calibrations; (iv) finally, as done here, to integrate data better from Earth and life sciences by focusing on the interdisciplinary study of the evolution of tropical African biodiversity in a wider geodiversity context.

Shrinking body sizes in response to warming: explanations for the temperature-size rule with special emphasis on the role of oxygen.

Abstract: Body size is central to ecology at levels ranging from organismal fecundity to the functioning of communities and ecosystems. Understanding temperature‐induced variations in body size is therefore of fundamental and applied interest, yet thermal responses of body size remain poorly understood. Temperature–size (T–S) responses tend to be negative (e.g. smaller body size at maturity when reared under warmer conditions), which has been termed the temperature–size rule (TSR). Explanations emphasize either physiological mechanisms (e.g. limitation of oxygen or other resources and temperature‐dependent resource allocation) or the adaptive value of either a large body size (e.g. to increase fecundity) or a short development time (e.g. in response to increased mortality in warm conditions). Oxygen limitation could act as a proximate factor, but we suggest it more likely constitutes a selective pressure to reduce body size in the warm: risks of oxygen limitation will be reduced as a consequence of evolution eliminating genotypes more prone to oxygen limitation. Thus, T–S responses can be explained by the ‘Ghost of Oxygen‐limitation Past’, whereby the resulting (evolved) T–S responses safeguard sufficient oxygen provisioning under warmer conditions, reflecting the balance between oxygen supply and demands experienced by ancestors. T–S responses vary considerably across species, but some of this variation is predictable. Body‐size reductions with warming are stronger in aquatic taxa than in terrestrial taxa. We discuss whether larger aquatic taxa may especially face greater risks of oxygen limitation as they grow, which may be manifested at the cellular level, the level of the gills and the whole‐organism level. In contrast to aquatic species, terrestrial ectotherms may be less prone to oxygen limitation and prioritize early maturity over large size, likely because overwintering is more challenging, with concomitant stronger end‐of season time constraints. Mechanisms related to time constraints and oxygen limitation are not mutually exclusive explanations for the TSR. Rather, these and other mechanisms may operate in tandem. But their relative importance may vary depending on the ecology and physiology of the species in question, explaining not only the general tendency of negative T–S responses but also variation in T–S responses among animals differing in mode of respiration (e.g. water breathers versus air breathers), genome size, voltinism and thermally associated behaviour (e.g. heliotherms).

Lakes in the era of global change: moving beyond single-lake thinking in maintaining biodiversity and ecosystem services.

Abstract: The Anthropocene presents formidable threats to freshwater ecosystems. Lakes are especially vulnerable and important at the same time. They cover only a small area worldwide but harbour high levels of biodiversity and contribute disproportionately to ecosystem services. Lakes differ with respect to their general type (e.g. land-locked, drainage, floodplain and large lakes) and position in the landscape (e.g. highland versus lowland lakes), which contribute to the dynamics of these systems. Lakes should be generally viewed as 'meta-systems', whereby biodiversity is strongly affected by species dispersal, and ecosystem dynamics are contributed by the flow of matter and substances among locations in a broader waterscape context. Lake connectivity in the waterscape and position in the landscape determine the degree to which a lake is prone to invasion by non-native species and accumulation of harmful substances. Highly connected lakes low in the landscape accumulate nutrients and pollutants originating from ecosystems higher in the landscape. The monitoring and restoration of lake biodiversity and ecosystem services should consider the fact that a high degree of dynamism is present at local, regional and global scales. However, local and regional monitoring may be plagued by the unpredictability of ecological phenomena, hindering adaptive management of lakes. Although monitoring data are increasingly becoming available to study responses of lakes to global change, we still lack suitable integration of models for entire waterscapes. Research across disciplinary boundaries is needed to address the challenges that lakes face in the Anthropocene because they may play an increasingly important role in harbouring unique aquatic biota as well as providing ecosystem goods and services in the future.

Assessing ontogenetic maturity in extinct saurian reptiles.

Abstract: Morphology forms the most fundamental level of data in vertebrate palaeontology because it is through interpretations of morphology that taxa are identified, creating the basis for broad evolutionary and palaeobiological hypotheses. Assessing maturity is one of the most basic aspects of morphological interpretation and provides the means to study the evolution of ontogenetic changes, population structure and palaeoecology, life-history strategies, and heterochrony along evolutionary lineages that would otherwise be lost to time. Saurian reptiles (the least-inclusive clade containing Lepidosauria and Archosauria) have remained an incredibly diverse, numerous, and disparate clade through their ~260-million-year history. Because of the great disparity in this group, assessing maturity of saurian reptiles is difficult, fraught with methodological and terminological ambiguity. We compiled a novel database of literature, assembling >900 individual instances of saurian maturity assessment, to examine critically how saurian maturity has been diagnosed. We review the often inexact and inconsistent terminology used in saurian maturity assessment (e.g. 'juvenile', 'mature') and provide routes for better clarity and cross-study coherence. We describe the various methods that have been used to assess maturity in every major saurian group, integrating data from both extant and extinct taxa to give a full account of the current state of the field and providing method-specific pitfalls, best practices, and fruitful directions for future research. We recommend that a new standard subsection, 'Ontogenetic Assessment', be added to the Systematic Palaeontology portions of descriptive studies to provide explicit ontogenetic diagnoses with clear criteria. Because the utility of different ontogenetic criteria is highly subclade dependent among saurians, even for widely used methods (e.g. neurocentral suture fusion), we recommend that phylogenetic context, preferably in the form of a phylogenetic bracket, be used to justify the use of a maturity assessment method. Different methods should be used in conjunction as independent lines of evidence when assessing maturity, instead of an ontogenetic diagnosis resting entirely on a single criterion, which is common in the literature. Critically, there is a need for data from extant taxa with well-represented growth series to be integrated with the fossil record to ground maturity assessments of extinct taxa in well-constrained, empirically tested methods.

Biodiversity as insurance: from concept to measurement and application

Abstract: Biological insurance theory predicts that, in a variable environment, aggregate ecosystem properties will vary less in more diverse communities because declines in the performance or abundance of some species or phenotypes will be offset, at least partly, by smoother declines or increases in others During the past two decades, ecology has accumulated strong evidence for the stabilising effect of biodiversity on ecosystem functioning As biological insurance is reaching the stage of a mature theory, it is critical to revisit and clarify its conceptual foundations to guide future developments, applications and measurements In this review, we first clarify the connections between the insurance and portfolio concepts that have been used in ecology and the economic concepts that inspired them Doing so points to gaps and mismatches between ecology and economics that could be filled profitably by new theoretical developments and new management applications Second, we discuss some fundamental issues in biological insurance theory that have remained unnoticed so far and that emerge from some of its recent applications In particular, we draw a clear distinction between the two effects embedded in biological insurance theory, ie the effects of biodiversity on the mean and variability of ecosystem properties This distinction allows explicit consideration of trade-offs between the mean and stability of ecosystem processes and services We also review applications of biological insurance theory in ecosystem management Finally, we provide a synthetic conceptual framework that unifies the various approaches across disciplines, and we suggest new ways in which biological insurance theory could be extended to address new issues in ecology and ecosystem management Exciting future challenges include linking the effects of biodiversity on ecosystem functioning and stability, incorporating multiple functions and feedbacks, developing new approaches to partition biodiversity effects across scales, extending biological insurance theory to complex interaction networks, and developing new applications to biodiversity and ecosystem management

How intelligent is a cephalopod? Lessons from comparative cognition.

Abstract: The soft-bodied cephalopods including octopus, cuttlefish, and squid are broadly considered to be the most cognitively advanced group of invertebrates. Previous research has demonstrated that these large-brained molluscs possess a suite of cognitive attributes that are comparable to those found in some vertebrates, including highly developed perception, learning, and memory abilities. Cephalopods are also renowned for performing sophisticated feats of flexible behaviour, which have led to claims of complex cognition such as causal reasoning, future planning, and mental attribution. Hypotheses to explain why complex cognition might have emerged in cephalopods suggest that a combination of predation, foraging, and competitive pressures are likely to have driven cognitive complexity in this group of animals. Currently, it is difficult to gauge the extent to which cephalopod behaviours are underpinned by complex cognition because many of the recent claims are largely based on anecdotal evidence. In this review, we provide a general overview of cephalopod cognition with a particular focus on the cognitive attributes that are thought to be prerequisites for more complex cognitive abilities. We then discuss different types of behavioural flexibility exhibited by cephalopods and, using examples from other taxa, highlight that behavioural flexibility could be explained by putatively simpler mechanisms. Consequently, behavioural flexibility should not be used as evidence of complex cognition. Fortunately, the field of comparative cognition centres on designing methods to pinpoint the underlying mechanisms that drive behaviours. To illustrate the utility of the methods developed in comparative cognition research, we provide a series of experimental designs aimed at distinguishing between complex cognition and simpler alternative explanations. Finally, we discuss the advantages of using cephalopods to develop a more comprehensive reconstruction of cognitive evolution.

The naked truth: a comprehensive clarification and classification of current ‘myths’ in naked mole-rat biology

Abstract: The naked mole-rat (Heterocephalus glaber) has fascinated zoologists for at least half a century. It has also generated considerable biomedical interest not only because of its extraordinary longevity, but also because of unusual protective features (e.g. its tolerance of variable oxygen availability), which may be pertinent to several human disease states, including ischemia/reperfusion injury and neurodegeneration. A recent article entitled 'Surprisingly long survival of premature conclusions about naked mole-rat biology' described 28 'myths' which, those authors claimed, are a 'perpetuation of beautiful, but falsified, hypotheses' and impede our understanding of this enigmatic mammal. Here, we re-examine each of these 'myths' based on evidence published in the scientific literature. Following Braude et al., we argue that these 'myths' fall into four main categories: (i) 'myths' that would be better described as oversimplifications, some of which persist solely in the popular press; (ii) 'myths' that are based on incomplete understanding, where more evidence is clearly needed; (iii) 'myths' where the accumulation of evidence over the years has led to a revision in interpretation, but where there is no significant disagreement among scientists currently working in the field; (iv) 'myths' where there is a genuine difference in opinion among active researchers, based on alternative interpretations of the available evidence. The term 'myth' is particularly inappropriate when applied to competing, evidence-based hypotheses, which form part of the normal evolution of scientific knowledge. Here, we provide a comprehensive critical review of naked mole-rat biology and attempt to clarify some of these misconceptions.

The biology of human hair greying.

Abstract: Hair greying (canities) is one of the earliest, most visible ageing-associated phenomena, whose modulation by genetic, psychoemotional, oxidative, senescence-associated, metabolic and nutritional factors has long attracted skin biologists, dermatologists, and industry. Greying is of profound psychological and commercial relevance in increasingly ageing populations. In addition, the onset and perpetuation of defective melanin production in the human anagen hair follicle pigmentary unit (HFPU) provides a superb model for interrogating the molecular mechanisms of ageing in a complex human mini-organ, and greying-associated defects in bulge melanocyte stem cells (MSCs) represent an intriguing system of neural crest-derived stem cell senescence. Here, we emphasize that human greying invariably begins with the gradual decline in melanogenesis, including reduced tyrosinase activity, defective melanosome transfer and apoptosis of HFPU melanocytes, and is thus a primary event of the anagen hair bulb, not the bulge. Eventually, the bulge MSC pool becomes depleted as well, at which stage greying becomes largely irreversible. There is still no universally accepted model of human hair greying, and the extent of genetic contributions to greying remains unclear. However, oxidative damage likely is a crucial driver of greying via its disruption of HFPU melanocyte survival, MSC maintenance, and of the enzymatic apparatus of melanogenesis itself. While neuroendocrine factors [e.g. alpha melanocyte-stimulating hormone (α-MSH), adrenocorticotropic hormone (ACTH), s-endorphin, corticotropin-releasing hormone (CRH), thyrotropin-releasing hormone (TRH)], and micropthalmia-associated transcription factor (MITF) are well-known regulators of human hair follicle melanocytes and melanogenesis, how exactly these and other factors [e.g. thyroid hormones, hepatocyte growth factor (HGF), P-cadherin, peripheral clock activity] modulate greying requires more detailed study. Other important open questions include how HFPU melanocytes age intrinsically, how psychoemotional stress impacts this process, and how current insights into the gerontobiology of the human HFPU can best be translated into retardation or reversal of greying.

The role of land-use history in driving successional pathways and its implications for the restoration of tropical forests.

Abstract: Secondary forests are increasingly important components of human-modified landscapes in the tropics. Successional pathways, however, can vary enormously across and within landscapes, with divergent regrowth rates, vegetation structure and species composition. While climatic and edaphic conditions drive variations across regions, land-use history plays a central role in driving alternative successional pathways within human-modified landscapes. How land use affects succession depends on its intensity, spatial extent, frequency, duration and management practices, and is mediated by a complex combination of mechanisms acting on different ecosystem components and at different spatial and temporal scales. We review the literature aiming to provide a comprehensive understanding of the mechanisms underlying the long-lasting effects of land use on tropical forest succession and to discuss its implications for forest restoration. We organize it following a framework based on the hierarchical model of succession and ecological filtering theory. This review shows that our knowledge is mostly derived from studies in Neotropical forests regenerating after abandonment of shifting cultivation or pasture systems. Vegetation is the ecological component assessed most often. Little is known regarding how the recovery of belowground processes and microbiota communities is affected by previous land-use history. In published studies, land-use history has been mostly characterized by type, without discrimination of intensity, extent, duration or frequency. We compile and discuss the metrics used to describe land-use history, aiming to facilitate future studies. The literature shows that (i) species availability to succession is affected by transformations in the landscape that affect dispersal, and by management practices and seed predation, which affect the composition and diversity of propagules on site. Once a species successfully reaches an abandoned field, its establishment and performance are dependent on resistance to management practices, tolerance to (modified) soil conditions, herbivory, competition with weeds and invasive species, and facilitation by remnant trees. (ii) Structural and compositional divergences at early stages of succession remain for decades, suggesting that early communities play an important role in governing further ecosystem functioning and processes during succession. Management interventions at early stages could help enhance recovery rates and manipulate successional pathways. (iii) The combination of local and landscape conditions defines the limitations to succession and therefore the potential for natural regeneration to restore ecosystem properties effectively. The knowledge summarized here could enable the identification of conditions in which natural regeneration could efficiently promote forest restoration, and where specific management practices are required to foster succession. Finally, characterization of the landscape context and previous land-use history is essential to understand the limitations to succession and therefore to define cost-effective restoration strategies. Advancing knowledge on these two aspects is key for finding generalizable relations that will increase the predictability of succession and the efficiency of forest restoration under different landscape contexts.

A conceptual framework of evolutionary novelty and innovation

Abstract: Since 1990 the recognition of deep homologies among metazoan developmental processes and the spread of more mechanistic approaches to developmental biology have led to a resurgence of interest in evolutionary novelty and innovation. Other evolutionary biologists have proposed central roles for behaviour and phenotypic plasticity in generating the conditions for the construction of novel morphologies, or invoked the accessibility of new regions of vast sequence spaces. These approaches contrast with more traditional emphasis on the exploitation of ecological opportunities as the primary source of novelty. This definitional cornucopia reflects differing stress placed on three attributes of novelties: their radical nature, the generation of new taxa, and ecological and evolutionary impact. Such different emphasis has led to conflating four distinct issues: the origin of novel attributes (genes, developmental processes, phenotypic characters), new functions, higher clades and the ecological impact of new structures and functions. Here I distinguish novelty (the origin of new characters, deep character transformations, or new combinations) from innovation, the ecological and evolutionary success of clades. Evidence from the fossil record of macroevolutionary lags between the origin of a novelty and its ecological success demonstrates that novelty may be decoupled from innovation, and only definitions of novelty based on radicality (rather than generativity or consequentiality) can be assessed without reference to the subsequent history of the clade to which a novelty belongs. These considerations suggest a conceptual framework for novelty and innovation, involving: (i) generation of the potential for novelty; (ii) the formation of novel attributes; (iii) refinement of novelties through adaptation; (iv) exploitation of novelties by a clade, which may coincide with a new round of ecological or environmental potentiation; followed by (v) the establishment of innovations through ecological processes. This framework recognizes that there is little empirical support for either the dominance of ecological opportunity, nor abrupt discontinuities (often caricatured as 'hopeful monsters'). This general framework may be extended to aspects of cultural and social innovation.

Wolbachia host shifts: routes, mechanisms, constraints and evolutionary consequences.

Abstract: Wolbachia is one of the most abundant endosymbionts on earth, with a wide distribution especially in arthropods. Effective maternal transmission and the induction of various phenotypes in their hosts are two key features of this bacterium. Here, we review our current understanding of another central aspect of Wolbachia's success: their ability to switch from one host species to another. We build on the proposal that Wolbachia host shifts occur in four main steps: (i) physical transfer to a new species; (ii) proliferation within that host; (iii) successful maternal transmission; and (iv) spread within the host species. Host shift can fail at each of these steps, and the likelihood of ultimate success is influenced by many factors. Some stem from traits of Wolbachia (different strains have different abilities for host switching), others on host features such as genetic resemblance (e.g. host shifting is likely to be easier between closely related species), ecological connections (the donor and recipient host need to interact), or the resident microbiota. Host shifts have enabled Wolbachia to reach its enormous current incidence and global distribution among arthropods in an epidemiological process shaped by loss and acquisition events across host species. The ability of Wolbachia to transfer between species also forms the basis of ongoing endeavours to control pests and disease vectors, following artificial introduction into uninfected hosts such as mosquitoes. Throughout, we emphasise the many knowledge gaps in our understanding of Wolbachia host shifts, and question the effectiveness of current methodology to detect these events. We conclude by discussing an apparent paradox: how can Wolbachia maintain its ability to undergo host shifts given that its biology seems dominated by vertical transmission?

Antarctic ecosystems in transition – life between stresses and opportunities

Abstract: Important findings from the second decade of the 21st century on the impact of environmental change on biological processes in the Antarctic were synthesised by 26 international experts. Ten key messages emerged that have stakeholder‐relevance and/or a high impact for the scientific community. They address (i) altered biogeochemical cycles, (ii) ocean acidification, (iii) climate change hotspots, (iv) unexpected dynamism in seabed‐dwelling populations, (v) spatial range shifts, (vi) adaptation and thermal resilience, (vii) sea ice related biological fluctuations, (viii) pollution, (ix) endangered terrestrial endemism and (x) the discovery of unknown habitats. Most Antarctic biotas are exposed to multiple stresses and considered vulnerable to environmental change due to narrow tolerance ranges, rapid change, projected circumpolar impacts, low potential for timely genetic adaptation, and migration barriers. Important ecosystem functions, such as primary production and energy transfer between trophic levels, have already changed, and biodiversity patterns have shifted. A confidence assessment of the degree of ‘scientific understanding’ revealed an intermediate level for most of the more detailed sub‐messages, indicating that process‐oriented research has been successful in the past decade. Additional efforts are necessary, however, to achieve the level of robustness in scientific knowledge that is required to inform protection measures of the unique Antarctic terrestrial and marine ecosystems, and their contributions to global biodiversity and ecosystem services.

How fire interacts with habitat loss and fragmentation.

Abstract: Biodiversity faces many threats and these can interact to produce outcomes that may not be predicted by considering their effects in isolation. Habitat loss and fragmentation (hereafter 'fragmentation') and altered fire regimes are important threats to biodiversity, but their interactions have not been systematically evaluated across the globe. In this comprehensive synthesis, including 162 papers which provided 274 cases, we offer a framework for understanding how fire interacts with fragmentation. Fire and fragmentation interact in three main ways: (i) fire influences fragmentation (59% of 274 cases), where fire either destroys and fragments habitat or creates and connects habitat; (ii) fragmentation influences fire (25% of cases) where, after habitat is reduced in area and fragmented, fire in the landscape is subsequently altered because people suppress or ignite fires, or there is increased edge flammability or increased obstruction to fire spread; and (iii) where the two do not influence each other, but fire interacts with fragmentation to affect responses like species richness, abundance and extinction risk (16% of cases). Where fire and fragmentation do influence each other, feedback loops are possible that can lead to ecosystem conversion (e.g. forest to grassland). This is a well-documented threat in the tropics but with potential also to be important elsewhere. Fire interacts with fragmentation through scale-specific mechanisms: fire creates edges and drives edge effects; fire alters patch quality; and fire alters landscape-scale connectivity. We found only 12 cases in which studies reported the four essential strata for testing a full interaction, which were fragmented and unfragmented landscapes that both span contrasting fire histories, such as recently burnt and long unburnt vegetation. Simulation and empirical studies show that fire and fragmentation can interact synergistically, multiplicatively, antagonistically or additively. These cases highlight a key reason why understanding interactions is so important: when fire and fragmentation act together they can cause local extinctions, even when their separate effects are neutral. Whether fire-fragmentation interactions benefit or disadvantage species is often determined by the species' preferred successional stage. Adding fire to landscapes generally benefits early-successional plant and animal species, whereas it is detrimental to late-successional species. However, when fire interacts with fragmentation, the direction of effect of fire on a species could be reversed from the effect expected by successional preferences. Adding fire to fragmented landscapes can be detrimental for species that would normally co-exist with fire, because species may no longer be able to disperse to their preferred successional stage. Further, animals may be attracted to particular successional stages leading to unexpected responses to fragmentation, such as higher abundance in more isolated unburnt patches. Growing human populations and increasing resource consumption suggest that fragmentation trends will worsen over coming years. Combined with increasing alteration of fire regimes due to climate change and human-caused ignitions, interactions of fire with fragmentation are likely to become more common. Our new framework paves the way for developing a better understanding of how fire interacts with fragmentation, and for conserving biodiversity in the face of these emerging challenges.

Two hundred years of zooplankton vertical migration research

Abstract: Vertical migration is a geographically and taxonomically widespread behaviour among zooplankton that spans across diel and seasonal timescales. The shorter-term diel vertical migration (DVM) has a periodicity of up to 1 day and was first described by the French naturalist Georges Cuvier in 1817. In 1888, the German marine biologist Carl Chun described the longer-term seasonal vertical migration (SVM), which has a periodicity of ca. 1 year. The proximate control and adaptive significance of DVM have been extensively studied and are well understood. DVM is generally a behaviour controlled by ambient irradiance, which allows herbivorous zooplankton to feed in food-rich shallower waters during the night when light-dependent (visual) predation risk is minimal and take refuge in deeper, darker waters during daytime. However, DVMs of herbivorous zooplankton are followed by their predators, producing complex predator-prey patterns that may be traced across multiple trophic levels. In contrast to DVM, SVM research is relatively young and its causes and consequences are less well understood. During periods of seasonal environmental deterioration, SVM allows zooplankton to evacuate shallower waters seasonally and take refuge in deeper waters often in a state of dormancy. Both DVM and SVM play a significant role in the vertical transport of organic carbon to deeper waters (biological carbon sequestration), and hence in the buffering of global climate change. Although many animal migrations are expected to change under future climate scenarios, little is known about the potential implications of global climate change on zooplankton vertical migrations and its impact on the biological carbon sequestration process. Further, the combined influence of DVM and SVM in determining zooplankton fitness and maintenance of their horizontal (geographic) distributions is not well understood. The contrasting spatial (deep versus shallow) and temporal (diel versus seasonal) scales over which these two migrations occur lead to challenges in studying them at higher spatial, temporal and biological resolution and coverage. Extending the largely population-based vertical migration knowledge base to individual-based studies will be an important way forward. While tracking individual zooplankton in their natural habitats remains a major challenge, conducting trophic-scale, high-resolution, year-round studies that utilise emerging field sampling and observation techniques, molecular genetic tools and computational hardware and software will be the best solution to improve our understanding of zooplankton vertical migrations.

Migration in butterflies: a global overview

Abstract: Insect populations including butterflies are declining worldwide, and they are becoming an urgent conservation priority in many regions Understanding which butterfly species migrate is critical to planning for their conservation, because management actions for migrants need to be coordinated across time and space Yet, while migration appears to be widespread among butterflies, its prevalence, as well as its taxonomic and geographic distribution are poorly understood The study of insect migration is hampered by their small size and the difficulty of tracking individuals over long distances Here we review the literature on migration in butterflies, one of the best-known insect groups We find that nearly 600 butterfly species show evidence of migratory movements Indeed, the rate of 'discovery' of migratory movements in butterflies suggests that many more species might in fact be migratory Butterfly migration occurs across all families, in tropical as well as temperate taxa; Nymphalidae has more migratory species than any other family (275 species), and Pieridae has the highest proportion of migrants (13%; 133 species) Some 13 lines of evidence have been used to ascribe migration status in the literature, but only a single line of evidence is available for 92% of the migratory species identified, with four or more lines of evidence available for only 10 species - all from the Pieridae and Nymphalidae Migratory butterflies occur worldwide, although the geographic distribution of migration in butterflies is poorly resolved, with most data so far coming from Europe, USA, and Australia Migration is much more widespread in butterflies than previously realised - extending far beyond the well-known examples of the monarch Danaus plexippus and the painted lady Vanessa cardui - and actions to conserve butterflies and insects in general must account for the spatial dependencies introduced by migratory movements

Social complexity and the fractal structure of group size in primate social evolution

Abstract: Compared to most other mammals and birds, anthropoid primates have unusually complex societies characterised by bonded social groups. Among primates, this effect is encapsulated in the social brain hypothesis: the robust correlation between various indices of social complexity (social group size, grooming clique size, tactical behaviour, coalition formation) and brain size. Hitherto, this has always been interpreted as a simple, unitary relationship. Using data for five different indices of brain volume from four independent brain databases, we show that the distribution of group size plotted against brain size is best described as a set of four distinct, very narrowly defined grades which are unrelated to phylogeny. The allocation of genera to these grades is highly consistent across the different data sets and brain indices. We show that these grades correspond to the progressive evolution of bonded social groups. In addition, we show, for those species that live in multilevel social systems, that the typical sizes of the different grouping levels in each case coincide with different grades. This suggests that the grades correspond to demographic attractors that are especially stable. Using five different cognitive indices, we show that the grades correlate with increasing social cognitive skills, suggesting that the cognitive demands of managing group cohesion increase progressively across grades. We argue that the grades themselves represent glass ceilings on animals' capacity to maintain social and spatial coherence during foraging and that, in order to evolve more highly bonded groups, species have to be able to invest in costly forms of cognition.

Surprisingly long survival of premature conclusions about naked mole-rat biology.

Abstract: Naked mole-rats express many unusual traits for such a small rodent. Their morphology, social behaviour, physiology, and ageing have been well studied over the past half-century. Many early findings and speculations about this subterranean species persist in the literature, although some have been repeatedly questioned or refuted. While the popularity of this species as a natural-history curiosity, and oversimplified story-telling in science journalism, might have fuelled the perpetuation of such misconceptions, an accurate understanding of their biology is especially important for this new biomedical model organism. We review 28 of these persistent myths about naked mole-rat sensory abilities, ecophysiology, social behaviour, development and ageing, and where possible we explain how these misunderstandings came about.

The biology and evolution of spider venoms.

Abstract: Spiders are diverse, predatory arthropods that have inhabited Earth for around 400 million years. They are well known for their complex venom systems that are used to overpower their prey. Spider venoms contain many proteins and peptides with highly specific and potent activities suitable for biomedical or agrochemical applications, but the key role of venoms as an evolutionary innovation is often overlooked, even though this has enabled spiders to emerge as one of the most successful animal lineages. In this review, we discuss these neglected biological aspects of spider venoms. We focus on the morphology of spider venom systems, their major components, biochemical and chemical plasticity, as well as ecological and evolutionary trends. We argue that the effectiveness of spider venoms is due to their unprecedented complexity, with diverse components working synergistically to increase the overall potency. The analysis of spider venoms is difficult to standardize because they are dynamic systems, fine-tuned and modified by factors such as sex, life-history stage and biological role. Finally, we summarize the mechanisms that drive spider venom evolution and highlight the need for genome-based studies to reconstruct the evolutionary history and physiological networks of spider venom compounds with more certainty.

Resolving the SLOSS dilemma for biodiversity conservation: a research agenda.

Abstract: The legacy of the 'SL > SS principle', that a single or a few large habitat patches (SL) conserve more species than several small patches (SS), is evident in decisions to protect large patches while down-weighting small ones. However, empirical support for this principle is lacking, and most studies find either no difference or the opposite pattern (SS > SL). To resolve this dilemma, we propose a research agenda by asking, 'are there consistent, empirically demonstrated conditions leading to SL > SS?' We first review and summarize 'single large or several small' (SLOSS) theory and predictions. We found that most predictions of SL > SS assume that between-patch variation in extinction rate dominates the outcome of the extinction-colonization dynamic. This is predicted to occur when populations in separate patches are largely independent of each other due to low between-patch movements, and when species differ in minimum patch size requirements, leading to strong nestedness in species composition along the patch size gradient. However, even when between-patch variation in extinction rate dominates the outcome of the extinction-colonization dynamic, theory can predict SS > SL. This occurs if extinctions are caused by antagonistic species interactions or disturbances, leading to spreading-of-risk of landscape-scale extinction across SS. SS > SL is also predicted when variation in colonization dominates the outcome of the extinction-colonization dynamic, due to higher immigration rates for SS than SL, and larger species pools in proximity to SS than SL. Theory that considers change in species composition among patches also predicts SS > SL because of higher beta diversity across SS than SL. This results mainly from greater environmental heterogeneity in SS due to greater variation in micro-habitats within and across SS habitat patches ('across-habitat heterogeneity'), and/or more heterogeneous successional trajectories across SS than SL. Based on our review of the relevant theory, we develop the 'SLOSS cube hypothesis', where the combination of three variables - between-patch movement, the role of spreading-of-risk in landscape-scale population persistence, and across-habitat heterogeneity - predict the SLOSS outcome. We use the SLOSS cube hypothesis and existing SLOSS empirical evidence, to predict SL > SS only when all of the following are true: low between-patch movement, low importance of spreading-of-risk for landscape-scale population persistence, and low across-habitat heterogeneity. Testing this prediction will be challenging, as it will require many studies of species groups and regions where these conditions hold. Each such study would compare gamma diversity across multiple landscapes varying in number and sizes of patches. If the prediction is not generally supported across such tests, then the mechanisms leading to SL > SS are extremely rare in nature and the SL > SS principle should be abandoned.

Speciation across the Tree of Life.

Abstract: Much of what we know about speciation comes from detailed studies of well-known model systems. Although there have been several important syntheses on speciation, few (if any) have explicitly compared speciation among major groups across the Tree of Life. Here, we synthesize and compare what is known about key aspects of speciation across taxa, including bacteria, protists, fungi, plants, and major animal groups. We focus on three main questions. Is allopatric speciation predominant across groups? How common is ecological divergence of sister species (a requirement for ecological speciation), and on what niche axes do species diverge in each group? What are the reproductive isolating barriers in each group? Our review suggests the following patterns. (i) Based on our survey and projected species numbers, the most frequent speciation process across the Tree of Life may be co-speciation between endosymbiotic bacteria and their insect hosts. (ii) Allopatric speciation appears to be present in all major groups, and may be the most common mode in both animals and plants, based on non-overlapping ranges of sister species. (iii) Full sympatry of sister species is also widespread, and may be more common in fungi than allopatry. (iv) Full sympatry of sister species is more common in some marine animals than in terrestrial and freshwater ones. (v) Ecological divergence of sister species is widespread in all groups, including ~70% of surveyed species pairs of plants and insects. (vi) Major axes of ecological divergence involve species interactions (e.g. host-switching) and habitat divergence. (vii) Prezygotic isolation appears to be generally more widespread and important than postzygotic isolation. (viii) Rates of diversification (and presumably speciation) are strikingly different across groups, with the fastest rates in plants, and successively slower rates in animals, fungi, and protists, with the slowest rates in prokaryotes. Overall, our study represents an initial step towards understanding general patterns in speciation across all organisms.

A paradigm shift in our view of species drives current trends in biological classification.

Abstract: Discontent about changes in species classifications has grown in recent years. Many of these changes are seen as arbitrary, stemming from unjustified conceptual and methodological grounds, or leading to species that are less distinct than those recognised in the past. We argue that current trends in species classification are the result of a paradigm shift toward which systematics and population genetics have converged and that regards species as the phylogenetic lineages that form the branches of the Tree of Life. Species delimitation now consists of determining which populations belong to which individual phylogenetic lineage. This requires inferences on the process of lineage splitting and divergence, a process to which we have only partial access through incidental evidence and assumptions that are themselves subject to refutation. This approach is not free of problems, as horizontal gene transfer, introgression, hybridisation, incorrect assumptions, sampling and methodological biases can mislead inferences of phylogenetic lineages. Increasing precision is demanded through the identification of both sister relationships and processes blurring or mimicking phylogeny, which has triggered, on the one hand, the development of methods that explicitly address such processes and, on the other hand, an increase in geographical and character data sampling necessary to infer/test such processes. Although our resolving power has increased, our knowledge of sister relationships - what we designate as species resolution - remains poor for many taxa and areas, which biases species limits and perceptions about how divergent species are or ought to be. We attribute to this conceptual shift the demise of trinominal nomenclature we are witnessing with the rise of subspecies to species or their rejection altogether; subspecies are raised to species if they are found to correspond to phylogenetic lineages, while they are rejected as fabricated taxa if they reflect arbitrary partitions of continuous or non-hereditary variation. Conservation strategies, if based on taxa, should emphasise species and reduce the use of subspecies to avoid preserving arbitrary partitions of continuous variation; local variation is best preserved by focusing on biological processes generating ecosystem resilience and diversity rather than by formally naming diagnosable units of any kind. Since many binomials still designate complexes of species rather than individual species, many species have been discovered but not named, geographical sampling is sparse, gene lineages have been mistaken for species, plenty of species limits remain untested, and many groups and areas lack adequate species resolution, we cannot avoid frequent changes to classifications as we address these problems. Changes will not only affect neglected taxa or areas, but also popular ones and regions where taxonomic research remained dormant for decades and old classifications were taken for granted.

Anticipated effects of abiotic environmental change on intraspecific social interactions.

Abstract: Social interactions are ubiquitous across the animal kingdom. A variety of ecological and evolutionary processes are dependent on social interactions, such as movement, disease spread, information transmission, and density-dependent reproduction and survival. Social interactions, like any behaviour, are context dependent, varying with environmental conditions. Currently, environments are changing rapidly across multiple dimensions, becoming warmer and more variable, while habitats are increasingly fragmented and contaminated with pollutants. Social interactions are expected to change in response to these stressors and to continue to change into the future. However, a comprehensive understanding of the form and magnitude of the effects of these environmental changes on social interactions is currently lacking. Focusing on four major forms of rapid environmental change currently occurring, we review how these changing environmental gradients are expected to have immediate effects on social interactions such as communication, agonistic behaviours, and group formation, which will thereby induce changes in social organisation including mating systems, dominance hierarchies, and collective behaviour. Our review covers intraspecific variation in social interactions across environments, including studies in both the wild and in laboratory settings, and across a range of taxa. The expected responses of social behaviour to environmental change are diverse, but we identify several general themes. First, very dry, variable, fragmented, or polluted environments are likely to destabilise existing social systems. This occurs as these conditions limit the energy available for complex social interactions and affect dissimilar phenotypes differently. Second, a given environmental change can lead to opposite responses in social behaviour, and the direction of the response often hinges on the natural history of the organism in question. Third, our review highlights the fact that changes in environmental factors are not occurring in isolation: multiple factors are changing simultaneously, which may have antagonistic or synergistic effects, and more work should be done to understand these combined effects. We close by identifying methodological and analytical techniques that might help to study the response of social interactions to changing environments, highlight consistent patterns among taxa, and predict subsequent evolutionary change. We expect that the changes in social interactions that we document here will have consequences for individuals, groups, and for the ecology and evolution of populations, and therefore warrant a central place in the study of animal populations, particularly in an era of rapid environmental change.

Nitrogen and phosphorus enrichment cause declines in invertebrate populations: a global meta-analysis

Abstract: Human-driven changes in nitrogen (N) and phosphorus (P) inputs are modifying biogeochemical cycles and the trophic state of many habitats worldwide. These alterations are predicted to continue to increase, with the potential for a wide range of impacts on invertebrates, key players in ecosystem-level processes. Here, we present a meta-analysis of 1679 cases from 207 studies reporting the effects of N, P, and combined N + P enrichment on the abundance, biomass, and richness of aquatic and terrestrial invertebrates. Nitrogen and phosphorus additions decreased invertebrate abundance in terrestrial and aquatic ecosystems, with stronger impacts under combined N + P additions. Likewise, N and N + P additions had stronger negative impacts on the abundance of tropical than temperate invertebrates. Overall, the effects of nutrient enrichment did not differ significantly among major invertebrate taxonomic groups, suggesting that changes in biogeochemical cycles are a pervasive threat to invertebrate populations across ecosystems. The effects of N and P additions differed significantly among invertebrate trophic groups but N + P addition had a consistent negative effect on invertebrates. Nutrient additions had weaker or inconclusive impacts on invertebrate biomass and richness, possibly due to the low number of case studies for these community responses. Our findings suggest that N and P enrichment affect invertebrate community structure mainly by decreasing invertebrate abundance, and these effects are dependent on the habitat and trophic identity of the invertebrates. These results highlight the important effects of human-driven nutrient enrichment on ecological systems and suggest a potential driver for the global invertebrate decline documented in recent years.

Deciphering the molecular mechanism of stop codon readthrough

Abstract: Recognition of the stop codon by the translation machinery is essential to terminating 12 translation at the right position and to synthesizing a protein of the correct size. Under certain 13 conditions, the stop codon can be recognized as a coding codon promoting translation, which 14 then terminates at a later stop codon. This event, called stop codon readthrough, occurs either 15 by error, due to a dedicated regulatory environment leading to generation of different protein 16 isoforms, or through the action of a readthrough compound. This review focuses on the 17 mechanisms of stop codon readthrough, the nucleotide and protein environments that 18 facilitate or inhibit it, and the therapeutic interest of stop codon readthrough in the treatment 19 of genetic diseases caused by nonsense mutations.

Artificial refuges for wildlife conservation: what is the state of the science?

Abstract: Artificial refuges are human-made structures that aim to create safe places for animals to breed, hibernate, or take shelter in lieu of natural refuges. Artificial refuges are used across the globe to mitigate the impacts of a variety of threats on wildlife, such as habitat loss and degradation. However, there is little understanding of the science underpinning artificial refuges, and what comprises best practice for artificial refuge design and implementation for wildlife conservation. We address this gap by undertaking a systematic review of the current state of artificial refuge research for the conservation of wildlife. We identified 224 studies of artificial refuges being implemented in the field to conserve wildlife species. The current literature on artificial refuges is dominated by studies of arboreal species, primarily birds and bats. Threatening processes addressed by artificial refuges were biological resource use (26%), invasive or problematic species (20%), and agriculture (15%), yet few studies examined artificial refuges specifically for threatened (Vulnerable, Endangered, or Critically Endangered) species (7%). Studies often reported the characteristics of artificial refuges (i.e. refuge size, construction materials; 87%) and surrounding vegetation (35%), but fewer studies measured the thermal properties of artificial refuges (18%), predator activity (17%), or food availability (3%). Almost all studies measured occupancy of the artificial refuges by target species (98%), and over half measured breeding activity (54%), whereas fewer included more detailed measures of fitness, such as breeding productivity (34%) or animal body condition (4%). Evaluating the benefits and impacts of artificial refuges requires sound experimental design, but only 39% of studies compared artificial refuges to experimental controls, and only 10% of studies used a before-after-control-impact (BACI) design. As a consequence, few studies of artificial refuges can determine their overall effect on individuals or populations. We outline a series of key steps in the design, implementation, and monitoring of artificial refuges that are required to avoid perverse outcomes and maximise the chances of achieving conservation objectives. This review highlights a clear need for increased rigour in studies of artificial refuges if they are to play an important role in wildlife conservation.

Convergence and divergence in lizard colour polymorphisms.

Abstract: Colour polymorphic species are model systems for examining the evolutionary processes that generate and maintain discrete phenotypic variation in natural populations. Lizards have repeatedly evolved strikingly similar polymorphic sexual signals in distantly related lineages, providing an opportunity to examine convergence and divergence in colour polymorphism, correlated traits and associated evolutionary processes. Herein, we synthesise the extensive literature on lizard colour polymorphisms in both sexes, including recent advances in understanding of the underlying biochemical, cellular and genetic mechanisms, and correlated behavioural, physiological and life-history traits. Male throat, head or ventral colour morphs generally consist of red/orange, yellow and white/blue morphs, and sometimes mixed morphs with combinations of two colours. Despite these convergent phenotypes, there is marked divergence in correlated behavioural, physiological and life-history traits. We discuss the need for coherence in morph classification, particularly in relation to 'mixed' morphs. We highlight future research directions such as the genetic basis of convergent phenotypes and the role of environmental variation in the maintenance of polymorphism. Research in this very active field promises to continue to provide novel insights with broad significance to evolutionary biologists.

Avian vocalisations: the female perspective.

Abstract: Research on avian vocalisations has traditionally focused on male song produced by oscine passerines. However, accumulating evidence indicates that complex vocalisations can readily evolve outside the traditional contexts of mate attraction and territory defence by male birds, and yet the previous bias towards male song has shaped - and continues to shape - our understanding of avian communication as a whole. Accordingly, in this review we seek to address this imbalance by synthesising studies on female vocalisations from across signalling contexts throughout the Aves, and discuss the implications of recent empirical advances for our understanding of vocalisations in both sexes. This review reveals great structural and functional diversity among female vocalisations and highlights the important roles that vocalisations can play in mediating female-specific behaviours. However, fundamental gaps remain. While there are now several case studies that identify the function of female vocalisations, few quantify the associated fitness benefits. Additionally, very little is known about the role of vocal learning in the development of female vocalisations. Thus, there remains a pressing need to examine the function and development of all forms of vocalisations in female birds. In the light of what we now know about the functions and mechanisms of female vocalisations, we suggest that conventional male-biased definitions of songs and calls are inadequate for furthering our understanding of avian vocal communication more generally. Therefore, we propose two simple alternatives, both emancipated from the sex of the singer. The first distinguishes song from calls functionally as a sexually selected vocal signal, whilst the second distinguishes them mechanistically in terms of their underlying neurological processes. It is clear that more investigations are needed into the ultimate and proximate causes of female vocalisations; however, these are essential if we are to develop a holistic epistemology of avian vocal communication in both sexes, across ecological contexts and taxonomic divides.

A roadmap to plant functional island biogeography

Abstract: Island biogeography is the study of the spatio-temporal distribution of species, communities, assemblages or ecosystems on islands and other isolated habitats. Island diversity is structured by five classes of process: dispersal, establishment, biotic interactions, extinction and evolution. Classical approaches in island biogeography focused on species richness as the deterministic outcome of these processes. This has proved fruitful, but species traits can potentially offer new biological insights into the processes by which island life assembles and why some species perform better at colonising and persisting on islands. Functional traits refer to morphological and phenological characteristics of an organism or species that can be linked to its ecological strategy and that scale up from individual plants to properties of communities and ecosystems. A baseline hypothesis is for traits and ecological strategies of island species to show similar patterns as a matched mainland environment. However, strong dispersal, environmental and biotic-interaction filters as well as stochasticity associated with insularity modify this baseline. Clades that do colonise often embark on distinct ecological and evolutionary pathways, some because of distinctive evolutionary forces on islands, and some because of the opportunities offered by freedom from competitors or herbivores or the absence of mutualists. Functional traits are expected to be shaped by these processes. Here, we review and discuss the potential for integrating functional traits into island biogeography. While we focus on plants, the general considerations and concepts may be extended to other groups of organisms. We evaluate how functional traits on islands relate to core principles of species dispersal, establishment, extinction, reproduction, biotic interactions, evolution and conservation. We formulate existing knowledge as 33 working hypotheses. Some of these are grounded on firm empirical evidence, others provide opportunities for future research. We organise our hypotheses under five overarching sections. Section A focuses on plant functional traits enabling species dispersal to islands. Section B discusses how traits help to predict species establishment, successional trajectories and natural extinctions on islands. Section C reviews how traits indicate species biotic interactions and reproduction strategies and which traits promote intra-island dispersal. Section D discusses how evolution on islands leads to predictable changes in trait values and which traits are most susceptible to change. Section E debates how functional ecology can be used to study multiple drivers of global change on islands and to formulate effective conservation measures. Islands have a justified reputation as research models. They illuminate the forces operating within mainland communities by showing what happens when those forces are released or changed. We believe that the lens of functional ecology can shed more light on these forces than research approaches that do not consider functional differences among species.

Towards an ecology of protective coloration.

Abstract: The strategies underlying different forms of protective coloration are well understood but little attention has been paid to the ecological, life-history and behavioural circumstances under which they evolve. While some comparative studies have investigated the ecological correlates of aposematism, and background matching, the latter particularly in mammals, few have examined the ecological correlates of other types of protective coloration. Here, we first outline which types of defensive coloration strategies may be exhibited by the same individual; concluding that many protective coloration mechanisms can be employed simultaneously, particularly in conjunction with background matching. Second, we review the ecological predictions that have been made for each sort of protective coloration mechanism before systematically surveying phylogenetically controlled comparative studies linking ecological and social variables to antipredator defences that involve coloration. We find that some a priori predictions based on small-scale empirical studies and logical arguments are indeed supported by comparative data, especially in relation to how illumination affects both background matching and self-shadow concealment through countershading; how body size is associated with countershading, motion dazzle, flash coloration and aposematism, although only in selected taxa; how immobility may promote background matching in ambush predators; and how mobility may facilitate motion dazzle. Examination of nearly 120 comparative tests reveals that many focus on ecological variables that have little to do with predictions derived from antipredator defence theory, and that broad-scale ecological studies of defence strategies that incorporate phylogenetics are still very much in their infancy. We close by making recommendations for future evolutionary ecological research.

Expanding insect pollinators in the Anthropocene

Abstract: Global changes are severely affecting pollinator insect communities worldwide, resulting in repeated patterns of species extirpations and extinctions. Whilst negative population trends within this functional group have understandably received much attention in recent decades, another facet of global changes has been overshadowed: species undergoing expansion. Here, we review the factors and traits that have allowed a fraction of the pollinating entomofauna to take advantage of global environmental change. Sufficient mobility, high resistance to acute heat stress, and inherent adaptation to warmer climates appear to be key traits that allow pollinators to persist and even expand in the face of climate change. An overall flexibility in dietary and nesting requirements is common in expanding species, although niche specialization can also drive expansion under specific contexts. The numerous consequences of wild and domesticated pollinator expansions, including competition for resources, pathogen spread, and hybridization with native wildlife, are also discussed. Overall, we show that the traits and factors involved in the success stories of expanding pollinators are mostly species specific and context dependent, rendering generalizations of 'winning traits' complicated. This work illustrates the increasing need to consider expansion and its numerous consequences as significant facets of global changes and encourages efforts to monitor the impacts of expanding insect pollinators, particularly exotic species, on natural ecosystems.