Breaking the Social–Non‐social Dichotomy: A Role for Reptiles in Vertebrate Social Behavior Research?

Although social behavior in vertebrates spans a continuum from solitary to highly social, taxa are often dichotomized as either ‘social’ or ‘non‐social’. We argue that this social dichotomy is overly simplistic, neglects the diversity of vertebrate social systems, impedes our understanding of the evolution of social behavior, and perpetuates the erroneous belief that one group—the reptiles—is primarily ‘non‐social’. This perspective essay highlights the diversity and complexity of reptile social systems, briefly reviews reasons for their historical neglect in research, and indicates how reptiles can contribute to our understanding of the evolution of vertebrate social behavior. Although a robust review of social behavior across vertebrates is lacking, the repeated evolution of social systems in multiple independent lineages enables investigation of the factors that promote shifts in vertebrate social behavior and the paraphyly of reptiles reinforces the need to understand reptile social behavior.     

An integrative model to predict maximum O2 uptake in animals with central vascular shunts

Gas exchange in the tissues and lungs is accurately described by simple equations, and mathematical models of O(2) transport play a paramount role in the conceptual understanding of respiratory physiology. In the present paper, we review an integrative approach to describe maximum oxygen uptake in animals with tidally ventilated lungs. Further, we expand the analysis by including a central vascular shunt compartment to mimic the cardiovascular anatomy of embryonic birds and mammals as well as many ectothermic vertebrates. Finally, we predict the effects of right-to-left and left-to-right cardiac shunts on maximal oxygen uptake and present a new hypothesis that relates the interaction of metabolic rates and central shunts in air breathing ectothermic vertebrates.     

The influence of host and non‐host companion plants on the behaviour of pest insects in field crops

Companion plants grown as ‘trap crops’ or ‘intercrops’ can be used to reduce insect infestations in field crops. The ways in which such reductions are achieved are being described currently using either a chemical approach, based on the ‘push‐pull strategy’, or a biological approach, based on the ‘appropriate/inappropriate landing theory’. The chemical approach suggests that insect numbers are reduced by chemicals from the intercrop ‘repelling’ insects from the main crop, and by chemicals from the trap‐crop ‘attracting’ insects away from the main crop. This approach is based on the assumptions that (1) plants release detectable amounts of volatile chemicals, and (2) insects ‘respond’ while still some distance away from the emitting plant. We discuss whether the above assumptions can be justified using the ‘appropriate/inappropriate landing theory’. Our tenet is that specialist insects respond only to the volatile chemicals released by their host plants and that these are released in such small quantities that, even with a heightened response to such chemicals, specialist insects can only detect them when a few metres from the emitting plant. We can find no robust evidence in the literature that plant chemicals ‘attract’ insects from more than 5 m and believe that ‘trap crops’ function simply as ‘interception barriers’. We can also find no evidence that insects are ‘repelled’ from landing on non‐host plants. Instead, we believe that ‘intercrops’ disrupt host‐plant finding by providing insects with a choice of host (appropriate) and non‐host (inappropriate) plant leaves on which to land, as our research has shown that, for intercropping to be effective, insects must land on the non‐host plants. Work is needed to determine whether non‐host plants are repellent (chemical approach) or ‘non‐stimulating’ (biological approach) to insects.     

Novel aspects of parenchymal–mesenchymal interactions: from cell types to molecules and beyond

Mesenchymal stem or stromal cells (MSCs) were initially isolated from the bone marrow and received their name on the basis of their ability to differentiate into multiple lineages such as bone, cartilage, fat and muscle. However, more recent studies suggest that MSCs residing in perivascular compartments of the small and large blood vessels play a regulatory function supporting physiologic and pathologic responses of parenchymal cells, which define the functional representation of an organ or tissue. MSCs secrete or express factors that reach neighbouring parenchymal cells via either a paracrine effect or a direct cell‐to‐cell interaction promoting functional activity, survival and proliferation of the parenchymal cells. Previous concept of ‘epithelial–stromal’ interactions can now be widened. Given that MSC can also support hematopoietic, neuronal and other non‐epithelial parenchymal lineages, terms ‘parenchymal–stromal’ or ‘parenchymal–mesenchymal’ interactions may better describe the supportive or ‘trophic’ functions of MSC. Importantly, in many cases, MSCs specifically provide supportive microenvironment for the most primitive stem or progenitor populations and therefore can play a role as ‘stem/progenitor niche’ forming cells. So far, regulatory roles of MSCs have been reported in many tissues. In this review article, we summarize the latest studies that focused on the supportive function of MSC. This thread of research leads to a new perspective on the interactions between parenchymal and mesenchymal cells and justifies a principally novel approach for regenerative medicine based on co‐application of MSC and parenchymal cell for the most efficient tissue repair. Copyright © 2013 John Wiley & Sons, Ltd.     

Microbial macroecology: highly structured prokaryotic soil assemblages in a tropical deciduous forest

Aim To assess the hypothesis that free‐living prokaryotes show a pattern of ‘no biogeography’ by examining the scaling of soil prokaryotic diversity and by comparing it with other groups’ biogeographical patterns. Location Two sites in the tropical deciduous forest of Chamela, Jalisco, on the western coast of Mexico. Methods We examined the diversity and distribution of soil prokaryotes in two 8 × 8 m quadrats divided in such manner that we could sample at four spatial scales. Restriction fragment length polymorphisms of 16S rRNA genes were used to define operational taxonomic units (OTUs) that we used in lieu of species to assess diversity. Results We found highly structured species assemblages that allowed us to reject multiple predictions of the hypothesis that soil bacteria show ‘no biogeography’. The frequency distribution of range size (measured as the occupancy of quadrats) of OTUs followed a hollow curve similar to that of vertebrates on continents. Assemblages showed high levels of beta diversity and a non‐random nested pattern of diversity. OTU diversity scaled with area followed a power function with slopes z = 0.42 and 0.47. Main conclusions We demonstrate a non‐ubiquitous dispersal for soil prokaryotes, which suggests a complex biogeography similar to that found for terrestrial vertebrates.     

Performance of Galia-type melons grafted on to Cucurbita rootstock in Monosporascus cannonballus-infested and non-infested soils

Galia‐type melons grafted on to the Cucurbita rootstock‘TZ 148’and non‐grafted controls were evaluated for vegetative development under greenhouse conditions. In general, the development of grafted and non‐grafted plants was similar within a cultivar. The horticultural and pathological performances of the Galia‐type melons ‘Carrera’, ‘NUN‐5554’, ‘6003’ and ‘Arava’ were evaluated in experiments conducted in non‐infested and Monosporascus‐infested soils. In non‐infested soil, grafted and non‐grafted ‘Carrera’, ‘NUN‐5554’ and ‘Arava’ had the same yields. The yield of grafted ‘6003’ was significantly higher than that of its non‐grafted control. Responses of grafted and non‐grafted Galia‐type melons to Monosporascus cannonballus were evaluated and compared in the spring and autumn growing seasons. Significant differences in disease incidence were found among cultivars, between grafted and non‐grafted plants, and between growing seasons. Disease reduction and the beneficial effect of grafting on yield were more pronounced in the spring. The results indicate that Galia‐type melons can be grafted successfully, but the cultivation of the grafted plants should be adapted to each growing area and season.     

Body size divergence in nine‐spined sticklebacks: disentangling additive genetic and maternal effects

Interpopulation differences in body size are of common occurrence in vertebrates, but the relative importance of genetic, maternal, and environmental effects as causes of observed differentiation have seldom been assessed in the wild. Gigantism in pond nine‐spined sticklebacks (Pungitius pungitius Linnaeus, 1758) has been repeatedly observed, but the quantitative genetic basis of population divergence in size has remained unstudied. We conducted a common garden experiment – using ‘pure’ and reciprocal crosses between two populations (‘giant’ pond versus ‘normal’ marine) – to test for the relative importance of additive genetic, non‐additive genetic, and maternal effects on body size after 11 months of growth in the laboratory. We found that body size difference between the two populations in laboratory conditions owed mainly to additive genetic effects, and only to a minor degree to maternal effects. Furthermore, the weak maternal effects were seen only in the offspring of ‘giant’ mothers, and appeared to be mediated through differences in egg size. Thus, the results suggest that gigantism in pond populations of P. pungitius is based on the effects of additively acting genes, rather than to direct environmental induction, or maternal or non‐additive gene action. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 107 , 521–528.     

When is dispersal for dispersal? Unifying marine and terrestrial perspectives

Recent syntheses on the evolutionary causes of dispersal have focused on dispersal as a direct adaptation, but many traits that influence dispersal have other functions, raising the question: when is dispersal ‘for’ dispersal? We review and critically evaluate the ecological causes of selection on traits that give rise to dispersal in marine and terrestrial organisms. In the sea, passive dispersal is relatively easy and specific morphological, behavioural, and physiological adaptations for dispersal are rare. Instead, there may often be selection to limit dispersal. On land, dispersal is relatively difficult without specific adaptations, which are relatively common. Although selection for dispersal is expected in both systems and traits leading to dispersal are often linked to fitness, systems may differ in the extent to which dispersal in nature arises from direct selection for dispersal or as a by‐product of selection on traits with other functions. Our analysis highlights incompleteness of theories that assume a simple and direct relationship between dispersal and fitness, not just insofar as they ignore a vast array of taxa in the marine realm, but also because they may be missing critically important effects of traits influencing dispersal in all realms.     

Interpreting multidimensionality in parasite‐induced phenotypic alterations: panselectionism versus parsimony

The purpose of this note is to provide an alternative to the interpretation of multidimensionality in parasite‐induced phenotypic alterations as a set of effectively‐independent traits produced by adaptive evolution. We propose here that infection with so‐called ‘manipulative parasites’ typically results in an ‘infection syndrome’, characterized by several distinctive symptoms corresponding to the alteration of particular phenotypic traits in infected hosts. Based on the available physiological evidence, we argue that symptoms might actually be the consequence of the dysregulation of some key neuromodulator, arising as a byproduct of the subversion of the host's immune system by the parasite. In that respect, it might be inadequate, from a functional point of view, to separate phenotypic effects that appear to increase trophic transmission from those that do not. We suggest that future research should test the validity of the ‘infection syndrome’ hypothesis through focusing on the mechanisms involved in multidimensionality at the intraspecific level, and through looking for the existence of non‐random associations between symptoms at the interspecific level, across host‐parasite associations.     

Density dependence in blowfly populations: experimental evaluation of non‐parametric time‐series modelling

Two approaches for describing density dependence in demographic rates of stage‐structured populations are compared in this study. Time‐series data from laboratory blowfly populations (Lucilia sericata) have been analysed in a separate study, with a statistical modelling approach that incorporated density dependences as unspecified (non‐parametric) functions. In this study, we assessed density‐dependent structures by manipulating densities of larvae and adults in cohorts of blowflies and measuring the demographic rates. We here compare the density‐dependent structures revealed by the cohort experiments with those estimated by the non‐parametric model. This model estimates the demographic rates to have the following density‐dependent structures: (i) larval survival was non‐linearly density‐dependent (a ‘humped’ function), (ii) adult survival was density‐independent, and (iii) reproductive rate decreased with adult density. In the cohort experiments reported here, (i) juvenile survival exhibited a positive density dependence in low densities (facilitation), which became negative at higher densities (competition). Pupal and adult size decreased with initial larval density. (ii) Adult survival was reduced by high initial larval density, but it was independent of adult density. (iii) Reproductive rate was reduced by high initial larval density, and by high adult density in populations of large individuals (from low larval density). Hence, the results from these experiments support the non‐parametric model estimates regarding density‐dependent structures of demographic rates in the blowfly populations. The mean demographic rates, however, were apparently underestimated by the model. We conclude that non‐parametric modelling is a useful first approach for exploratory analysis of ecological time‐series data.     

Building a new research framework for social evolution: intralocus caste antagonism

The breeding and non‐breeding ‘castes’ of eusocial insects provide a striking example of role‐specific selection, where each caste maximises fitness through different morphological, behavioural and physiological trait values. Typically, queens are long‐lived egg‐layers, while workers are short‐lived, largely sterile foragers. Remarkably, the two castes are nevertheless produced by the same genome. The existence of inter‐caste genetic correlations is a neglected consequence of this shared genome, potentially hindering the evolution of caste dimorphism: alleles that increase the productivity of queens may decrease the productivity of workers and vice versa, such that each caste is prevented from reaching optimal trait values. A likely consequence of this ‘intralocus caste antagonism’ should be the maintenance of genetic variation for fitness and maladaptation within castes (termed ‘caste load’), analogous to the result of intralocus sexual antagonism. The aim of this review is to create a research framework for understanding caste antagonism, drawing in part upon conceptual similarities with sexual antagonism. By reviewing both the social insect and sexual antagonism literature, we highlight the current empirical evidence for caste antagonism, discuss social systems of interest, how antagonism might be resolved, and challenges for future research. We also introduce the idea that sexual and caste antagonism could interact, creating a three‐way antagonism over gene expression. This includes unpacking the implications of haplodiploidy for the outcome of this complex interaction.     

Beyond blasphemy or devotion: art,the secular,and Catholicism in Paris

In this article I explore the relationship between the secular and ‘cultural’ Catholicism in France through the lens of a contemporary art exhibit displayed at a new project of the French Catholic Church. Visitors’ varied responses to the exhibit, I argue, ultimately reinforced the organizers’ claim that the activities that occur within this ‘non‐religious’ space of the French church are self‐evident aspects of a broadly recognizable and ‘secular’ French or European culture.     

P2X receptors mediated abnormal interaction between satellite glial cells and neurons in visceral pathological changes

The adenosine triphosphate (ATP)‐gated P2X receptor cation channel family consists of permeable ligand‐gated ion channels that expand on the binding of extracellular adenosine 5’‐ATP. ATP‐gated P2X receptors are trimer ion channels that assemble homo or isomer from seven cloned subunits. P2X receptors are discovered mostly in mammalian and are being found in an increasing number of non‐vertebrates, such as zebrafish, bullfrog, and ameba. P2X receptors are involved in many physiological processes, including regulation of heart rhythm and contractility, and regulation of pain, especially chronic pain and glia integration. This review summarizes the current studies on the regulation of P2X receptors in abnormal neuronal‐glial interaction and the pathological changes in viscera, especially in myocardial ischemia.     

An evolutionary perspective on the systems of adaptive immunity

We propose an evolutionary perspective to classify and characterize the diverse systems of adaptive immunity that have been discovered across all major domains of life. We put forward a new function‐based classification according to the way information is acquired by the immune systems: Darwinian immunity (currently known from, but not necessarily limited to, vertebrates) relies on the Darwinian process of clonal selection to ‘learn’ by cumulative trial‐and‐error feedback; Lamarckian immunity uses templated targeting (guided adaptation) to internalize heritable information on potential threats; finally, shotgun immunity operates through somatic mechanisms of variable targeting without feedback. We argue that the origin of Darwinian (but not Lamarckian or shotgun) immunity represents a radical innovation in the evolution of individuality and complexity, and propose to add it to the list of major evolutionary transitions. While transitions to higher‐level units entail the suppression of selection at lower levels, Darwinian immunity re‐opens cell‐level selection within the multicellular organism, under the control of mechanisms that direct, rather than suppress, cell‐level evolution for the benefit of the individual. From a conceptual point of view, the origin of Darwinian immunity can be regarded as the most radical transition in the history of life, in which evolution by natural selection has literally re‐invented itself. Furthermore, the combination of clonal selection and somatic receptor diversity enabled a transition from limited to practically unlimited capacity to store information about the antigenic environment. The origin of Darwinian immunity therefore comprises both a transition in individuality and the emergence of a new information system – the two hallmarks of major evolutionary transitions. Finally, we present an evolutionary scenario for the origin of Darwinian immunity in vertebrates. We propose a revival of the concept of the ‘Big Bang’ of vertebrate immunity, arguing that its origin involved a ‘difficult’ (i.e. low‐probability) evolutionary transition that might have occurred only once, in a common ancestor of all vertebrates. In contrast to the original concept, we argue that the limiting innovation was not the generation of somatic diversity, but the regulatory circuitry needed for the safe operation of amplifiable immune responses with somatically acquired targeting. Regulatory complexity increased abruptly by genomic duplications at the root of the vertebrate lineage, creating a rare opportunity to establish such circuitry. We discuss the selection forces that might have acted at the origin of the transition, and in the subsequent stepwise evolution leading to the modern immune systems of extant vertebrates.     

The stress response and immune system share,borrow, and reconfigure their physiological network elements: Evidence from the insects

The classic biomedical view is that stress hormone effects on the immune system are largely pathological, especially if the stress is chronic. However, more recent interpretations have focused on the potential adaptive function of these effects. This paper examines stress response-immune system interactions from a physiological network perspective, using insects because of their simpler physiology. For example, stress hormones can reduce disease resistance, yet activating an immune response results in the release of stress hormones in both vertebrates and invertebrates. From a network perspective, this phenomenon is consistent with the ‘sharing’ of the energy-releasing ability of stress hormones by both the stress response and the immune system. Stress-induced immunosuppression is consistent with the stress response ‘borrowing’ molecular components from the immune system to increase the capacity of stress-relevant physiological processes (i.e. a trade off). The insect stress hormones octopamine and adipokinetic hormone can also ‘reconfigure’ the immune system to help compensate for the loss of some of the immune system's molecular resources (e.g. apolipophorin III). This view helps explain seemingly maladaptive interactions between the stress response and immune system. The adaptiveness of stress hormone effects on individual immune components may be apparent only from the perspective of the whole organism. These broad principles will apply to both vertebrates and invertebrates.     

Ready to Fight: Reliable Predictors of Attack in a Cooperatively Breeding,Non‐Passerine Bird

Signal reliability is a major focus of animal communication research. Aggressive signals are ideal for measuring signal reliability because the signal referent – attack or no attack – can be measured unambiguously. Signals of aggressive intent occur at elevated rates in aggressive contexts, predict subsequent aggression by the signaler, and elicit appropriate responses from receivers. We tested the ‘predictive criterion’ in smooth‐billed anis, Crotophaga ani, by broadcasting one of two playback types (‘ahnee’ calls only or ‘ahnee + hoot’ calls), presenting a taxidermic mount, and observing the animals’ behavior. Based on the hypotheses that ‘hoot’ calls and ‘throat‐inflation’ displays signal aggressive intent, we predicted that they would be associated with attack, and that signaling rate would increase over the time period leading up to an attack. Indeed, both hoots and throat‐inflation displays reliably predicted attack. The second prediction, that signaling rate increases in the time leading up to attack, was strongly supported for throat‐inflation displays, which increased over the pre‐attack period in both treatments. Hoots increased over the pre‐attack period in ahnee playbacks but not in ahnee + hoot playbacks. Hierarchical signaling systems are characterized by early, less‐reliable predictors of attack, and later, more reliable predictors of attack. During both natural and simulated interactions, the more‐reliable throat‐inflation display tended to precede the less‐reliable hoot call, suggesting that this signaling system is not hierarchical. In a comparison of 11 putative signals of aggressive intent in birds, the throat‐inflation display had the second highest mutual information (reduction in uncertainty) among visual signals and non‐passerine signals while hoots had below‐average mutual information. Natural observations indicate that both hoots and throat‐inflation displays occur in the context of aggressive between‐group encounters, and hoots also occur during within‐group interactions. Throat‐inflation displays appear to be reliable indicators of aggressive intent, but the function of hoot calls is less clear.     

Effect of dung beetle species richness and chemical perturbation on multiple ecosystem functions

1. The relationship between biodiversity and ecosystem functioning is typically positive but saturating, suggesting widespread functional redundancy within ecological communities. However, theory predicts that apparent redundancy can be reduced or removed when systems are perturbed, or when multifunctionality (the simultaneous delivery of multiple functions) is considered. 2. Manipulative experiments were used to test whether higher levels of dung beetle species richness enhanced individual functions and multifunctionality, and whether these relationships were influenced by perturbation (in this case, non‐target exposure to the veterinary anthelmintic ivermectin). The four ecosystem functions tested were dung removal, primary productivity, soil faunal feeding activity and reduction in soil bulk density. 3. For individual functions, perturbation had limited effects on functioning, with only dung removal significantly (negatively) affected. Species richness did not, on its own, explain significant variation in the delivery of individual functions. In the case of primary productivity, an interaction between richness and perturbation was found: species‐rich dung beetle assemblages enhanced forage growth in the unperturbed treatment, relative to the perturbed treatment. 4. Using a composite ‘multifunctionality index’ it was found that species‐rich dung beetle assemblages delivered marginally higher levels of multifunctionality in unperturbed conditions; however, this benefit was lost under perturbation. Using a relatively new and robust method of assessing diversity–multifunctionality relationships across a range of thresholds, no significant effect of species richness on multifunctionality was found.     

Expanding on Watson's framework for classifying patches: when is an island not an island?

Aim The aims were: (1) evaluate the potential of Watson's framework for studying species composition in fragments and islands for a specific landscape type: cryptobiotic crust systems in the arid south‐western US; (2) expand Watson's original model to include ephemeral/non‐equilibrium systems by revising his categories of patch age and matrix contrast; and (3) examine the interplay between patch dynamics and species autecology, demonstrating the need for more work on ephemeral patchy systems. Location Cryptobiotic crust systems in two piñon‐juniper sites in Central New Mexico, western North America. Results Watson's patch age designation was not applicable to our system because of its ephemeral or non‐equilibrial nature. Based on this result, we constructed what we refer to as a ‘speed key’ that includes equilibrium and non‐equilibrium patches of all kinds. For this model we maintained one of Watson's original traits: patch origin, and amended two others to describe persistence and permeability across the matrix. Importantly, persistence and matrix permeability must be evaluated as functions of the organisms under consideration. Systems that may be in equilibrium for one taxon may well be non‐equilibrial (ephemeral) for another. A patch that appears to be in high contrast with its intervening matrix may actually be in low contrast, depending on the dispersal ability of the organism through that matrix. Main conclusions To improve substantially on our understanding of patchy systems (whether islands or fragments) it is important to account explicitly for relevant organismal life‐history traits in the designation of those systems. Too often, patches are defined by how the researcher views them from his/her own spatio‐temporal viewpoint. Once we move to an organism‐centred understanding of these patches we may find surprising and novel comparisons that allow us to move across scales and inform our view of ecological patterns and processes. By incorporating non‐equilibrium systems into a model of insularity, this work has general implications that go beyond the scope of cryptobiotic crusts to add to the current dialogue in biogeography.     

Habitat amount hypothesis and passive sampling explain mammal species composition in Amazonian river islands

Nested structures of species assemblages have been frequently associated with patch size and isolation, leading to the conclusion that colonization–extinction dynamics drives nestedness. The ‘passive sampling’ model states that the regional abundance of species randomly determines their occurrence in patches. The ‘habitat amount hypothesis’ also challenges patch size and isolation effects, arguing that they occur because of a ‘sample area effect’. Here, we (a) ask whether the structure of the mammal assemblages of fluvial islands shows a nested pattern, (b) test whether species’ regional abundance predicts species’ occurrence on islands, and (c) ask whether habitat amount in the landscape and matrix resistance to biological flow predict the islands’ species composition. We quantified nestedness and tested its significance using null models. We used a regression model to analyze whether a species’ relative regional abundance predicts its incidence on islands. We accessed islands’ species composition by an NMDS ordination and used multiple regression to evaluate how species composition responds to habitat amount and matrix resistance. The degree of nestedness did not differ from that expected by the passive sampling hypothesis. Likewise, species’ regional abundance predicted its occurrence on islands. Habitat amount successfully predicted the species composition on islands, whereas matrix resistance did not. We suggest the application of habitat amount hypothesis for predicting species composition in other patchy systems. Although the island biogeography perspective has dominated the literature, we suggest that the passive sampling perspective is more appropriate for explaining the assemblages’ structure in this and other non‐equilibrium patch systems. Abstract in Portuguese is available with online material.     

Can current velocity mediate trophic cascades in a mountain stream?

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