Increased susceptibility to fungal disease accompanies adaptation to drought in Brassica rapa

Recent studies have demonstrated adaptive evolutionary responses to climate change, but little is known about how these responses may influence ecological interactions with other organisms, including natural enemies. We used a resurrection experiment in the greenhouse to examine the effect of evolutionary responses to drought on the susceptibility of Brassica rapa plants to a fungal pathogen, Alternaria brassicae. In agreement with previous studies in this population, we found an evolutionary shift to earlier flowering postdrought, which was previously shown to be adaptive. Here, we report the novel finding that postdrought descendant plants were also more susceptible to disease, indicating a rapid evolutionary shift to increased susceptibility. This was accompanied by an evolutionary shift to increased specific leaf area (thinner leaves) following drought. We found that flowering time and disease susceptibility displayed plastic responses to experimental drought treatments, but that this plasticity did not match the direction of evolution, indicating that plastic and evolutionary responses to changes in climate can be opposed. The observed evolutionary shift to increased disease susceptibility accompanying adaptation to drought provides evidence that even if populations can rapidly adapt in response to climate change, evolution in other traits may have ecological effects that could make species more vulnerable.     

The action of stabilizing selection on the perfection of new characters in evolution

In birds, fusion of the carpal elements to a carpometacarpus during morphogenesis takes place during the evolutionary process at different rates, i.e. heterochronically, in different groups (developmental radiations), like the elements of the nasal apparatus in Sauropsida. This is because new characters spread and are pushed back at different rates from the terminal to the initial levels of morphogenesis. The shift is most likely automatic, in that it does not require further mutation, but it is set in motion by selection. Selection does not take effect only when an adequate character (which at first is very imperfect) is accepted; it also causes the character to grow, pushes it back towards the threshold of morphogenesis and thereby increases its perfection and its fitness. The path along which the shift takes place is determined by the morphogenetic route of recapitulation of the ancestral structure and since this movement is caused by protracted stabilizing selection, we can describe it as orthoselective movement. This means that recapitulation is flexible. At the same time, cellular and epigenetic interactions with surrounding structures are reciprocally influenced. The shift continues until adequate adaptation and perfection have been achieved. Stabilizing selection then ceases to act. The shift shows the evolutionary trend or further developmental possibilities. Its chief role is probably in the development of specializations.     

PEAK SHIFTS PRODUCED BY CORRELATED RESPONSE TO SELECTION

Traits may evolve both as a consequence of direct selection and also as a correlated response to selection on other traits. While correlated response may be important for both the production of evolutionary novelty and in the build-up of complex characters, its potential role in peak shifts has been neglected empirically and theoretically. We use a quantitative genetic model to investigate the conditions under which a character, Y, which has two alternative optima, can be dragged from one optimum to the other as a correlated response to selection on a second character, X. High genetic correlations between the two characters make the transition, or peak shift, easier, as does weak selection tending to restore Y to the optimum from which it is being dragged. When selection on Y is very weak, the conditions for a peak shift depend only on the location of the new optimum for X and are independent of the strength of selection moving it there. Thus, if the “adaptive valley” for Y is very shallow, little reduction in mean fitness is needed to produce a shift. If the selection acts strongly to keep Y at its current optimum, very intense directional selection on X, associated with a dramatic drop in mean fitness, is required for a peak shift. When strong selection is required, the conditions for peak shifts driven by correlated response might occur rarely, but still with sufficient frequency on a geological timescale to be evolutionarily important.     

The theory of increasing autonomy in evolution: a proposal for understanding macroevolutionary innovations

Attempts to explain the origin of macroevolutionary innovations have been only partially successful. Here it is proposed that the patterns of major evolutionary transitions have to be understood first, before it is possible to further analyse the forces behind the process. The hypothesis is that major evolutionary innovations are characterized by an increase in organismal autonomy, in the sense of emancipation from the environment. After a brief overview of the literature on this subject, increasing autonomy is defined as the evolutionary shift in the individual system–environment relationship, such that the direct influences of the environment are gradually reduced and a stabilization of self-referential, intrinsic functions within the system is generated. This is described as relative autonomy because numerous interconnections with the environment and dependencies upon it are retained. Features of increasing autonomy are spatial separations, an increase in homeostatic functions and in body size, internalizations and an increase in physiological and behavioral flexibility. It is described how these features are present in different combinations in the major evolutionary transitions of metazoans and, consequently, how they should be taken into consideration when evolutionary innovations are studied. The hypothesis contributes to a reconsideration of the relationship between organisms and their environment.     

Modularity, comparative embryology and evo-devo: Developmental dissection of evolving body plans

Modules can be defined as quasi-autonomous units that are connected loosely with each other within a system. A need for the concept of modularity has emerged as we deal with evolving organisms in evolutionary developmental research, especially because it is unknown how genes are associated with anatomical patterns. One of the strategies to link genotypes with phenotypes could be to relate developmental modules with morphological ones. To do this, it is fundamental to grasp the context in which certain anatomical units and developmental processes are associated with each other specifically. By identifying morphological modularities as units recognized by some categories of general homology as established by comparative anatomy, it becomes possible to identify developmental modules whose genetic components exhibit coextensive expressions. This permits us to distinguish the evolutionary modification in which the identical morphological module simply alters its shape for adaptation, without being decoupled from the functioning gene network (‘coupled modularities’), from the evolution of novelty that involves a heterotopic shift between the anatomical and developmental modules. Using this formulation, it becomes possible, within the realm of Geoffroy's homologous networks, to reduce morphological homologies to developmental mechanistic terms by dissociating certain classes of modules that are often associated with actual shapes and functions.     

The demographic transition: are we any closer to an evolutionary explanation?

The radical shift in human reproduction in the late 19th century, known as the demographic transition, constitutes a major challenge to evolutionary approaches to human behaviour. Why would people ever choose to limit their reproduction voluntarily when, at the peak of the Industrial Revolution, resources were apparently so plentiful? Can the transition be attributed to standard life history tradeoffs, is it a consequence of cultural evolutionary processes, or is it simply a maladaptive outcome of novel and environmental social conditions? Empirical analyses and new models suggest that reproductive decision making might be driven by a human psychology designed by natural selection to maximize material wealth. If this is the case, the mechanisms governing fertility and parental investment are likely to respond to modern conditions with a fertility level much lower than that that would maximize fitness.     

What is resource partitioning?

The concept of resource partitioning, as originally developed, relates to evolutionary change in species in response to selection pressures generated by interspecific competition. More recently it has taken on another meaning, one that is not defined in terms of evolutionary function, and which refers simply to differences in resource use between species regardless of the origins of the differences. Such a shift in usage has several drawbacks for ecological theory, which are discussed. Of most practical significance to ecologists is the inappropriate justification conferred on the continued use of a category that contains characters that are not equivalents. Ecologists are therefore frequently in the position of explaining the presence of species in an area by reference to the by-products of their adaptive evolution.     

Ecological and evolutionary responses in complex communities: implications for invasions and eco‐evolutionary feedbacks

It is easier to predict the ecological and evolutionary outcomes of interactions in less diverse communities. As species are added to communities, their direct and indirect interactions multiply, their niches may shift, and there may be increased ecological redundancy. Accompanying this complexity in ecological interactions, is also complexity in selection and subsequent evolution, which may feed back to affect the ecology of the system, as species with different traits may play different ecological roles. Drawing from my own work and that of many others, I first discuss what we currently understand about ecology and evolution in light of simple and diverse communities, and suggest the importance of escape from community complexity per se in the success of invaders. Then, I examine how community complexity may influence the nature and magnitude of eco‐evolutionary feedbacks, classifying eco‐evolutionary dynamics into three general types: those generating alternative stable states, cyclic dynamics, and those maintaining ecological stasis and stability. The latter may be important and yet very hard to detect. I suggest future directions, as well as discuss methodological approaches and their potential pitfalls, in assessing the importance and longevity of eco‐evolutionary feedbacks in complex communities. Synthesis The ecology, evolution and eco‐evolutionary dynamics of simple and diverse communities are reviewed. In more diverse communities, direct and indirect interactions multiply, species’ niches often shift, ecological redundancy can increase, and selection may be less directional. Community complexity may influence the magnitude and nature of eco‐evolutionary dynamics, which are classified into three types: those generating alternative stable states, cyclic dynamics, and those maintaining ecological stasis and stability. Strengths and pitfalls of approaches to investigating eco‐evolutionary feedbacks in complex field communities are discussed.     

CLEAVAGE PATTERNS AND MESENTOBLAST FORMATION IN THE GASTROPODA: AN EVOLUTIONARY PERSPECTIVE

The larger gastropod taxa are characterized by distinctive cleavage patterns. The cell stage at which the mesentoblast is formed appears to be crucial. In none of the taxa is it formed earlier than the 24- and not later than the 63-cell stage. A heterochronic shift from late to early mesentoblast formation appears to coincide with successive steps in gastropod evolution. Comparison of the early cleavage patterns appears to be a powerful method for investigating the evolutionary relations between major gastropod taxa.     

Host shift and cospeciation rate estimation from co‐phylogenies

Host shifts can cause novel infectious diseases, and is a key process in diversification. Disentangling the effects of host shift vs. those of cospeciation is non‐trivial as both can result in phylogenic congruence. We develop a new framework based on network analysis and Approximate Bayesian Computation to quantify host shift and cospeciation rates in host‐parasite systems. Our method enables estimation of the expected time to the next host shift or cospeciation event. We then apply it to avian haemosporidian parasite systems and to the pocket gophers‐chewing lice system, and demonstrate that both host shift and cospeciation can be reliably estimated by our method. We confirm that host shifts have shaped the evolutionary history of avian haemosporidian parasites and have played a minor role in the gopher–chewing lice system. Our method is promising for predicting the rate of potential host shifts and thus the emergence of novel infectious diseases.     

Finding the frame shift: digit loss, developmental variability, and the origin of the avian hand

The origin of the tridactyl hand of crown birds from the pentadactyl hand of those early theropod dinosaurs lying along the avian stem has become a classic, but at times seemingly intractable, historical problem. The point in question is whether the fingers of crown birds represent digits 1-3 as predicted by generalized trends in the fossil record; or digits 2-4, as evidenced by the topology of the embryonic mesenchymal condensations from which the digits develop. The frame shift hypothesis attempted to resolve this paradox by making these signals congruent by means of a homeotic transformation in digital identity, but recently the paleontological support for this hypothesis was questioned. Here, we reassess the frame shift from a paleontological perspective by addressing what predictions a frame shift makes for skeletal morphology, whether the frame shift remains a viable explanation of the known fossil data, and where on the theropod tree the frame shift most likely occurred. Our results indicate that the frame shift remains viable, and based on the inferred pattern of digit loss, the frame shift likely occurred at a deeper position in theropod phylogeny than previously proposed. A new evolutionary model of the frame shift is described in which the early history of the frame-shifted hand is marked by an extended zone of developmental polymorphism. This model provides a new conceptual framework for the role of developmental variability in communicating broad evolutionary patterns on a taxonomically inclusive phylogenetic tree.     

Parallel adaptations to nectarivory in parrots,key innovations and the diversification of the Loriinae

Specialization to nectarivory is associated with radiations within different bird groups, including parrots. One of them, the Australasian lories, were shown to be unexpectedly species rich. Their shift to nectarivory may have created an ecological opportunity promoting species proliferation. Several morphological specializations of the feeding tract to nectarivory have been described for parrots. However, they have never been assessed in a quantitative framework considering phylogenetic nonindependence. Using a phylogenetic comparative approach with broad taxon sampling and 15 continuous characters of the digestive tract, we demonstrate that nectarivorous parrots differ in several traits from the remaining parrots. These trait‐changes indicate phenotype–environment correlations and parallel evolution, and may reflect adaptations to feed effectively on nectar. Moreover, the diet shift was associated with significant trait shifts at the base of the radiation of the lories, as shown by an alternative statistical approach. Their diet shift might be considered as an evolutionary key innovation which promoted significant non‐adaptive lineage diversification through allopatric partitioning of the same new niche. The lack of increased rates of cladogenesis in other nectarivorous parrots indicates that evolutionary innovations need not be associated one‐to‐one with diversification events.     

The use and abuse of Darwinian psychology: Its impact on attempts to determine the evolutionary basis of human rape

This paper evaluates the impact of the recent theoretical shift to Darwinian psychology on attempts to determine the evolutionary basis of human rape. The first step in this evaluation is a summary of the debate over whether human rape is an adaptation or a by-product of other evolved differences between men and women as it was presented in a pre-Darwinian psychological framework. These early evolutionary explanations are then contrasted with more recent works addressing the same issue from the perspective of Darwinian psychology. It is concluded that while the new approach may have helped generate new predictions, it has also led to the unwarranted exclusion of relevant data, led to questionable interpretations of new types of data, introduced ambiguous jargon, and potentially jeopardized the testability of certain evolutionary explanations. The root of most of these problems is suggested to exist, not in the principles of Darwinian psychology, but in the exaggeration of the differences between Darwinian psychology and earlier evolutionary approaches.     

Peak shift discrimination learning as a mechanism of signal evolution

"Peak shift" is a behavioral response bias arising from discrimination learning in which animals display a directional, but limited, preference for or avoidance of unusual stimuli. Its hypothesized evolutionary relevance has been primarily in the realm of aposematic coloration and limited sexual dimorphism. Here, we develop a novel functional approach to peak shift, based on signal detection theory, which characterizes the response bias as arising from uncertainty about stimulus appearance, frequency, and quality. This approach allows the influence of peak shift to be generalized to the evolution of signals in a variety of domains and sensory modalities. The approach is illustrated with a bumblebee (Bombus impatiens) discrimination learning experiment. Bees exhibited peak shift while foraging in an artificial Batesian mimicry system. Changes in flower abundance, color distribution, and visitation reward induced bees to preferentially visit novel flower colors that reduced the risk of flower-type misidentification. Under conditions of signal uncertainty, peak shift results in visitation to rarer, but more easily distinguished, morphological variants of rewarding species in preference to their average morphology. Peak shift is a common and taxonomically widespread phenomenon. This example of the possible role of peak shift in signal evolution can be generalized to other systems in which a signal receiver learns to make choices in situations in which signal variation is linked to the sender's reproductive success.     

A major shift in diversification rate helps explain macroevolutionary patterns in primate species diversity

Primates represent one of the most species rich, wide ranging, and ecologically diverse clades of mammals. What major macroevolutionary factors have driven their diversification and contributed to the modern distribution of primate species remains widely debated. We employed phylogenetic comparative methods to examine the role of clade age and evolutionary rate heterogeneity in the modern distribution of species diversity of Primates. Primate diversification has accelerated since its origin, with decreased extinction leading to a shift to even higher evolutionary rates in the most species rich family (Cercopithecidae). Older primate clades tended to be more diverse, however a shift in evolutionary rate was necessary to adequately explain the imbalance in species diversity. Species richness was also poorly explained by geographic distribution, especially once clade age and evolutionary rate shifts were accounted for, and may relate instead to other ecological factors. The global distribution of primate species diversity appears to have been strongly impacted by heterogeneity in evolutionary rates.     

From success to persistence: Identifying an evolutionary regime shift in the diverse Paleozoic aquatic arthropod group Eurypterida,driven by the Devonian biotic crisis

Mass extinctions have altered the trajectory of evolution a number of times over the Phanerozoic. During these periods of biotic upheaval a different selective regime appears to operate, although it is still unclear whether consistent survivorship rules apply across different extinction events. We compare variations in diversity and disparity across the evolutionary history of a major Paleozoic arthropod group, the Eurypterida. Using these data, we explore the group's transition from a successful, dynamic clade to a stagnant persistent lineage, pinpointing the Devonian as the period during which this evolutionary regime shift occurred. The late Devonian biotic crisis is potentially unique among the “Big Five” mass extinctions in exhibiting a drop in speciation rates rather than an increase in extinction. Our study reveals eurypterids show depressed speciation rates throughout the Devonian but no abnormal peaks in extinction. Loss of morphospace occupation is random across all Paleozoic extinction events; however, differential origination during the Devonian results in a migration and subsequent stagnation of occupied morphospace. This shift appears linked to an ecological transition from euryhaline taxa to freshwater species with low morphological diversity alongside a decrease in endemism. These results demonstrate the importance of the Devonian biotic crisis in reshaping Paleozoic ecosystems.     

The innovation triad: an EvoDevo agenda

This article introduces a special issue on evolutionary innovation and morphological novelty, two interrelated themes that have received a remarkable increase of attention over the past few years. We begin with a discussion of the question of whether innovation and novelty represent distinct evolutionary problems that require a distinct conceptualization. We argue that the mechanisms of innovation and their phenotypic results--novelty--can only be properly addressed if they are distinguished from the standard evolutionary themes of variation and adaptation, and we present arguments for making such a distinction. We propose that origination, the first formation of biological structures, is another distinct problem of morphological evolution, and that together with innovation and novelty it constitutes a conceptual complex we call the innovation triad. We define a problem agenda of the triad, which separates the analysis of the initiating conditions from the mechanistic realization of innovation, and we discuss the theoretical problems that arise from treating innovation as distinct from variation. Further, we categorize the empirical approaches that address themes of the innovation triad in recognizing four major strands of research: the morphology and systematics program, the gene regulation program, the epigenetic program, and the theoretical biology program. We provide examples of each program, giving priority to contributions in the present issue. In conclusion, we observe that the innovation triad is one of the defining topics of EvoDevo research and may represent its most pertinent contribution to evolutionary theory. We point out that an inclusion of developmental systems properties into evolutionary theory represents a shift of explanatory emphasis from the external factors of natural selection to the internal dynamics of developmental systems, complementing adaptation with emergence, and contingency with inherency.     

Cooperation,clumping and the evolution of multicellularity

The evolution of multicellular organisms represents one of the major evolutionary transitions in the history of life. A potential advantage of forming multicellular clumps is that it provides an efficiency benefit to pre-existing cooperation, such as the production of extracellular ‘public goods’. However, this is complicated by the fact that cooperation could jointly evolve with clumping, and clumping could have multiple consequences for the evolution of cooperation. We model the evolution of clumping and a cooperative public good, showing that (i) when considered separately, both clumping and public goods production gradually increase with increasing genetic relatedness; (ii) in contrast, when the traits evolve jointly, a small increase in relatedness can lead to a major shift in evolutionary outcome—from a non-clumping state with low public goods production to a cooperative clumping state with high values of both traits; (iii) high relatedness makes it easier to get to the cooperative clumping state and (iv) clumping can be inhibited when it increases the number of cells that the benefits of cooperation must be shared with, but promoted when it increases relatedness between those cells. Overall, our results suggest that public goods sharing can facilitate the formation of well-integrated cooperative clumps as a first step in the evolution of multicellularity.     

SEXUAL PARTNERS FOR THE STRESSED: FACULTATIVE OUTCROSSING IN THE SELF-FERTILIZING NEMATODE CAENORHABDITIS ELEGANS

Sexual reproduction shuffles genetic variation, potentially enhancing the evolutionary response to environmental change. Many asexual organisms respond to stress by generating facultative sexual reproduction, presumably as a means of escaping the trap of low genetic diversity. Self-fertilizing organisms are subject to similar genetic limitations: the consistent loss of genetic diversity within lineages restricts the production of variation through recombination. Selfing organisms may therefore benefit from a similar shift in mating strategy during periods of stress. We determined the effects of environmental stress via starvation and passage through the stress-resistant dauer stage on mating system dynamics of Caenorhabditis elegans , which reproduces predominantly through self-fertilization but is capable of outcrossing in the presence of males. Starvation elevated male frequencies in a strain-specific manner through differential male survival during dauer exposure and increased outcrossing rates after dauer exposure. In the most responsive strain, the mating system changed from predominantly selfing to almost exclusively outcrossing. Like facultative sex in asexual organisms, facultative outcrossing in C. elegans may periodically facilitate adaptation under stress. Such a shift in reproductive strategy should have a major impact on evolutionary change within these populations and may be a previously unrecognized feature of other highly selfing organisms.     

Embryonic cleavage cycles: how is a mouse like a fly?

The evolutionary advent of uterine support of embryonic growth in mammals is relatively recent. Nonetheless, striking differences in the earliest steps of embryogenesis make it difficult to draw parallels even with other chordates. We suggest that use of fertilization as a reference point misaligns the earliest stages and masks parallels that are evident when development is aligned at conserved stages surrounding gastrulation. In externally deposited eggs from representatives of all the major phyla, gastrulation is preceded by specialized extremely rapid cleavage cell cycles. Mammals also exhibit remarkably fast cell cycles in close association with gastrulation, but instead of beginning development with these rapid cycles, the mammalian egg first devotes itself to the production of extraembryonic structures. Previous attempts to identify common features of cleavage cycles focused on post-fertilization divisions of the mammalian egg. We propose that comparison to the rapid peri-gastrulation cycles is more appropriate and suggest that these cycles are related by evolutionary descent to the early cleavage stages of embryos such as those of frog and fly. The deferral of events in mammalian embryogenesis might be due to an evolutionary shift in the timing of fertilization.