Does wing reduction influence the relationship between altitude and insect body size? A case study using New Zealand's diverse stonefly fauna

Researchers have long been intrigued by evolutionary processes that explain biological diversity. Numerous studies have reported strong associations between animal body size and altitude, but insect analyses have often yielded equivocal results. Here, we analyze a collection database of New Zealand's diverse endemic stonefly fauna (106 species across 21 genera) to test for relationships between altitude and plecopteran body size. This insect assemblage includes a variety of wing‐reduced (26 spp) and fully winged (80 spp) taxa and covers a broad range of altitudes (0–2,000 m). We detected significant relationships between altitude and body size for wing‐reduced, but not fully winged, stonefly taxa. These results suggest that, while the maintenance of flight apparatus might place a constraint on body size in some fully winged species, the loss of flight may free insects from this evolutionary constraint. We suggest that rapid switches in insect dispersal ability may facilitate rapid evolutionary shifts across a number of biological attributes and may explain the inconsistent results from previous macroecological analyses of insect assemblages.     

Rapid Parallel Adaptation to Anthropogenic Heavy Metal Pollution

The impact of human-mediated environmental change on the evolutionary trajectories of wild organisms is poorly understood. In particular, capacity of species to adapt rapidly (in hundreds of generations or less), reproducibly and predictably to extreme environmental change is unclear. Silene uniflora is predominantly a coastal species, but it has also colonized isolated, disused mines with phytotoxic, zinc-contaminated soils. To test whether rapid, parallel adaptation to anthropogenic pollution has taken place, we used reduced representation sequencing (ddRAD) to reconstruct the evolutionary history of geographically proximate mine and coastal population pairs and found largely independent colonization of mines from different coastal sites. Furthermore, our results show that parallel evolution of zinc tolerance has occurred without gene flow spreading adaptive alleles between mine populations. In genomic regions where signatures of selection were detected across multiple mine-coast pairs, we identified genes with functions linked to physiological differences between the putative ecotypes, although genetic differentiation at specific loci is only partially shared between mine populations. Our results are consistent with a complex, polygenic genetic architecture underpinning rapid adaptation. This shows that even under a scenario of strong selection and rapid adaptation, evolutionary responses to human activities (and other environmental challenges) may be idiosyncratic at the genetic level and, therefore, difficult to predict from genomic data.     

PHYTOPHAGOUS INSECT–MICROBE MUTUALISMS AND ADAPTIVE EVOLUTIONARY DIVERSIFICATION

Adaptive diversification is a process intrinsically tied to species interactions. Yet, the influence of most types of interspecific interactions on adaptive evolutionary diversification remains poorly understood. In particular, the role of mutualistic interactions in shaping adaptive radiations has been largely unexplored, despite the ubiquity of mutualisms and increasing evidence of their ecological and evolutionary importance. Our aim here is to encourage empirical inquiry into the relationship between mutualism and evolutionary diversification, using herbivorous insects and their microbial mutualists as exemplars. Phytophagous insects have long been used to test theories of evolutionary diversification; moreover, the diversification of a number of phytophagous insect lineages has been linked to mutualisms with microbes. In this perspective, we examine microbial mutualist mediation of ecological opportunity and ecologically based divergent natural selection for their insect hosts. We also explore the conditions and mechanisms by which microbial mutualists may either facilitate or impede adaptive evolutionary diversification. These include effects on the availability of novel host plants or adaptive zones, modifying host-associated fitness trade-offs during host shifts, creating or reducing enemy-free space, and, overall, shaping the evolution of ecological (host plant) specialization. Although the conceptual framework presented here is built on phytophagous insect–microbe mutualisms, many of the processes and predictions are broadly applicable to other mutualisms in which host ecology is altered by mutualistic interactions.     

Phytophagous insect-microbe mutualisms and adaptive evolutionary diversification.

Adaptive diversification is a process intrinsically tied to species interactions. Yet, the influence of most types of interspecific interactions on adaptive evolutionary diversification remains poorly understood. In particular, the role of mutualistic interactions in shaping adaptive radiations has been largely unexplored, despite the ubiquity of mutualisms and increasing evidence of their ecological and evolutionary importance. Our aim here is to encourage empirical inquiry into the relationship between mutualism and evolutionary diversification, using herbivorous insects and their microbial mutualists as exemplars. Phytophagous insects have long been used to test theories of evolutionary diversification; moreover, the diversification of a number of phytophagous insect lineages has been linked to mutualisms with microbes. In this perspective, we examine microbial mutualist mediation of ecological opportunity and ecologically based divergent natural selection for their insect hosts. We also explore the conditions and mechanisms by which microbial mutualists may either facilitate or impede adaptive evolutionary diversification. These include effects on the availability of novel host plants or adaptive zones, modifying host-associated fitness trade-offs during host shifts, creating or reducing enemy-free space, and, overall, shaping the evolution of ecological (host plant) specialization. Although the conceptual framework presented here is built on phytophagous insect-microbe mutualisms, many of the processes and predictions are broadly applicable to other mutualisms in which host ecology is altered by mutualistic interactions.     

Rapid genome‐wide evolution in Brassica rapa populations following drought revealed by sequencing of ancestral and descendant gene pools

There is increasing evidence that evolution can occur rapidly in response to selection. Recent advances in sequencing suggest the possibility of documenting genetic changes as they occur in populations, thus uncovering the genetic basis of evolution, particularly if samples are available from both before and after selection. Here, we had a unique opportunity to directly assess genetic changes in natural populations following an evolutionary response to a fluctuation in climate. We analysed genome‐wide differences between ancestors and descendants of natural populations of Brassica rapa plants from two locations that rapidly evolved changes in multiple phenotypic traits, including flowering time, following a multiyear late‐season drought in California. These ancestor‐descendant comparisons revealed evolutionary shifts in allele frequencies in many genes. Some genes showing evolutionary shifts have functions related to drought stress and flowering time, consistent with an adaptive response to selection. Loci differentiated between ancestors and descendants (F_ST outliers) were generally different from those showing signatures of selection based on site frequency spectrum analysis (Tajima's D), indicating that the loci that evolved in response to the recent drought and those under historical selection were generally distinct. Very few genes showed similar evolutionary responses between two geographically distinct populations, suggesting independent genetic trajectories of evolution yielding parallel phenotypic changes. The results show that selection can result in rapid genome‐wide evolutionary shifts in allele frequencies in natural populations, and highlight the usefulness of combining resurrection experiments in natural populations with genomics for studying the genetic basis of adaptive evolution.     

Evolutionary consequences of climate‐induced range shifts in insects

Range shifts can rapidly create new areas of geographic overlap between formerly allopatric taxa and evidence is accumulating that this can affect species persistence. We review the emerging literature on the short‐ and long‐term consequences of these geographic range shifts. Specifically, we focus on the evolutionary consequences of novel species interactions in newly created sympatric areas by describing the potential (i) short‐term processes acting on reproductive barriers between species and (ii) long‐term consequences of range shifts on the stability of hybrid zones, introgression and ultimately speciation and extinction rates. Subsequently, we (iii) review the empirical literature on insects to evaluate which processes have been studied, and (iv) outline some areas that deserve increased attention in the future, namely the genomics of hybridisation and introgression, our ability to forecast range shifts and the impending threat from insect vectors and pests on biodiversity, human health and crop production. Our review shows that species interactions in de novo sympatric areas can be manifold, sometimes increasing and sometimes decreasing species diversity. A key issue that emerges is that climate‐induced hybridisations in insects are much more widespread than anticipated and that rising temperatures and increased anthropogenic disturbances are accelerating the process of species mixing. The existing evidence only shows the tip of the iceberg and we are likely to see many more cases of species mixing following range shifts in the near future.     

Anthropogenic evolution in an insect wing polymorphism following widespread deforestation

Anthropogenic environmental change can underpin major shifts in natural selective regimes, and can thus alter the evolutionary trajectories of wild populations. However, little is known about the evolutionary impacts of deforestation—one of the most pervasive human-driven changes to terrestrial ecosystems globally. Absence of forest cover (i.e. exposure) has been suggested to play a role in selecting for insect flightlessness in montane ecosystems. Here, we capitalize on human-driven variation in alpine treeline elevation in New Zealand to test whether anthropogenic deforestation has caused shifts in the distributions of flight-capable and flightless phenotypes in a wing-polymorphic lineage of stoneflies from the Zelandoperla fenestrata species complex. Transect sampling revealed sharp transitions from flight-capable to flightless populations with increasing elevation. However, these phenotypic transitions were consistently delineated by the elevation of local treelines, rather than by absolute elevation, providing a novel example of human-driven evolution in response to recent deforestation. The inferred rapid shifts to flightlessness in newly deforested regions have implications for the evolution and conservation of invertebrate biodiversity.     

Terrestrial insects and climate change: adaptive responses in key traits

Understanding and predicting how adaptation will contribute to species' resilience to climate change will be paramount to successfully managing biodiversity for conservation, agriculture, and human health‐related purposes. Making predictions that capture how species will respond to climate change requires an understanding of how key traits and environmental drivers interact to shape fitness in a changing world. Current trait‐based models suggest that low‐ to mid‐latitude populations will be most at risk, although these models focus on upper thermal limits, which may not be the most important trait driving species' distributions and fitness under climate change. In this review, we discuss how different traits (stress, fitness and phenology) might contribute and interact to shape insect responses to climate change. We examine the potential for adaptive genetic and plastic responses in these key traits and show that, although there is evidence of range shifts and trait changes, explicit consideration of what underpins these changes, be that genetic or plastic responses, is largely missing. Despite little empirical evidence for adaptive shifts, incorporating adaptation into models of climate change resilience is essential for predicting how species will respond under climate change. We are making some headway, although more data are needed, especially from taxonomic groups outside of Drosophila, and across diverse geographical regions. Climate change responses are likely to be complex, and such complexity will be difficult to capture in laboratory experiments. Moving towards well designed field experiments would allow us to not only capture this complexity, but also study more diverse species.     

<Emphasis Type="Italic">Drosophila</Emphasis> as models to understand the adaptive process during invasion

The last few decades have seen a growing number of species invasions globally, including many insect species. In drosophilids, there are several examples of successful invasions, i.e. Zaprionus indianus and Drosophila subobscura some decades ago, but the most recent and prominent example is the invasion of Europe and North America by the pest species, Drosophila suzukii. During the invasive process, species often encounter diverse environmental conditions that they must respond to, either through rapid genetic adaptive shifts or phenotypic plasticity, or by some combination of both. Consequently, invasive species constitute powerful models for investigating various questions related to the adaptive processes that underpin successful invasions. In this paper, we highlight how Drosophila have been and remain a valuable model group for understanding these underlying adaptive processes, and how they enable insight into key questions in invasion biology, including how quickly adaptive responses can occur when species are faced with new environmental conditions.     

Ecology and speciation

Recent studies on diverse taxa suggest that natural selection caused by shifts in ecology or invasions of novel habitats plays an important role in adaptive divergence and speciation. Exciting new studies integrating approaches from both the field and the laboratory suggest that ecological shifts can result in extremely rapid rates of evolutionary divergence. Although experimental approaches that link rapid ecological divergence to reproductive isolation and speciation are in their infancy, recent research indicates those approaches that will be most useful.     

Natural selection on the Drosophila antimicrobial immune system

The evolutionary dynamics of immune defenses have long attracted interest because of the special role the immune system plays in mediating the antagonistic interaction between hosts and pathogens. The antimicrobial immune system of the fruit fly Drosophila melanogaster is genetically well characterized and serves as a valuable model for studying insect and human innate immune defenses. I review here evolutionary and comparative genomic analyses of insect antimicrobial immune genes, with an emphasis on Drosophila. Core signal transduction pathways in the immune system are orthologously conserved across long evolutionary distances, but genes in these pathways evolve rapidly and adaptively at the amino acid sequence level. By contrast, families of genes encoding antimicrobial peptides are remarkably dynamic in genomic duplication and deletion, yet individual genes show little indication of adaptive sequence evolution. Pattern recognition receptors that trigger humoral immunity are evolutionarily rather static, but receptors required for phagocytosis show considerable genomic rearrangement and adaptive sequence divergence. The distinct evolutionary patterns exhibited by these various classes of immune system genes can be logically connected to the functions of the proteins they encode.     

Genetic and epigenetic alterations after hybridization and genome doubling

Hybridization and polyploidization are now recognized as major phenomena in the evolution of plants, promoting genetic diversity, adaptive radiation and speciation. Modern molecular techniques have recently provided evidence that allopolyploidy can induce several types of genetic and epigenetic events that are of critical importance for the evolutionary success of hybrids: (1) chromosomal rearrangements within one or both parental genomes contribute toward proper meiotic pairing and isolation of the hybrid from its progenitors; (2) demethylation and activation of dormant transposable elements may trigger insertional mutagenesis and changes in local patterns of gene expression, facilitating rapid genomic reorganisation; (3) rapid and reproducible loss of low copy DNA sequence appears to result in further differentiation of homoeologous chromosomes; and (4) organ-specific up- or down-regulation of one of the duplicated genes, resulting in unequal expression or silencing one copy. All these alterations also have the potential, while stabilizing allopolyploid genomes, to produce novel expression patterns and new phenotypes, which together with increased heterozygosity and gene redundancy might confer on hybrids an elevated evolutionary potential, with effects at scales ranging from molecular to ecological. Although important advances have been made in understanding genomic responses to allopolyploidization, further insights are still expected to be gained in the near future, such as the direction and nature of the diploidization process, functional relevance of gene expression alterations, molecular mechanisms that result in adaptation to different ecologies/habitats, and ecological and evolutionary implications of recurrent polyploidization.     

Rapid responses to a strong experimental selection for heat hardening in the invasive whitefly Bemisia tabaci MEAM 1

Adaptation to new environments is an important issue for invasive species as colonization depends on evolvability in their new distribution range. Here, we considered the case of the whitefly Bemisia tabaci MEAM 1 (Gennadius) (Hemiptera: Aleyrodidae), a pest that has recently invaded Colombia and where thermal adaptation has been proposed to explain its colonizing ability. An experimental evolution study was conducted to assess the evolutionary potential of B. tabaci in relation to its upper thermal limits, to explain its rapid adaptation during post‐invasion periods. Selection for hardening capacity was conducted in four whitefly populations. We measured thermal responses in relation to fitness components (survival, fecundity, and viability) for 5–7 generations under a strong selection regime. Heat hardening responded rapidly in both sexes. This was expressed as an increase in survival, but not in fecundity or viability. These results suggest that thermal responses for heat hardening are not correlated and evolve independently. Increased survival after few generations of selection points to high adaptive potential in this insect, which leads to rapid post‐invasion adaptation. Our study can help to predict population responses to environmental change and explain the colonizing ability of this pest.     

A meta-analysis of adaptive deme formation in phytophagous insect populations

The adaptive deme formation (ADF) hypothesis predicts that herbivorous insects become locally adapted to their host plants over time. Since its inception, approximately 17 independent studies have tested ADF, and they are divided in support and rejection of the hypothesis. This field of insect evolutionary ecology has a contentious history, and the contradictory studies obscure our understanding of the general evolutionary importance of adaptive deme formation in phytophagous insects. We conducted a meta-analysis in an attempt to clarify this issue. Meta-analysis is a statistical method for quantitatively comparing and synthesizing the results of different studies in a way that is more objective than a traditional literature review. Our analysis indicates that local adaptation is an important phenomenon in diverse insect systems. Contrary to predictions of the original hypothesis, there was no evidence that insect dispersal ability, and ostensibly gene flow, was associated with local adaptive differentiation. There was some indication that breeding (parthenogenetic, haplodiploid, diplodiploid) and feeding (exophagous, endophagous) modes may influence the evolution of locally adapted demes. Our analysis supports the theory of adaptive deme formation and provides guidance for future research directions.     

Do arms races punctuate evolutionary stasis? Unified insights from phylogeny,phylogeography and microevolutionary processes

One of the major controversies in evolutionary biology concerns the processes underlying macroevolutionary patterns in which prolonged stasis is disrupted by rapid, short-term evolution that leads species to new adaptive zones. Recent advances in the understanding of contemporary evolution have suggested that such rapid evolution can occur in the wild as a result of environmental changes. Here, we examined a novel hypothesis that evolutionary stasis is punctuated by co-evolutionary arms races, which continuously alter adaptive peaks and landscapes. Based on the phylogeny of long-mouthed weevils in the genus Curculio , likelihood ratio tests showed that the macroevolutionary pattern of the weevils coincides with the punctuational evolution model. A coalescent analysis of a species, Curculio camelliae , the mouthpart of which has diverged considerably among populations because of an arms race with its host plant, further suggested that major evolutionary shifts had occurred within 7000 generations. Through a microevolutionary analysis of the species, we also found that natural selection acting through co-evolutionary interactions is potentially strong enough to drive rapid evolutionary shifts between adaptive zones. Overall, we posit that co-evolution is an important factor driving the history of organismal evolution.     

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.     

Temporal shifts as elusive responses to anthropogenic stressors in a mammal community

Conservation decision-making often relies on species’ distribution changes in response to anthropogenic disturbances but overlook their temporal responses. Filling the knowledge gap on the temporal shifts as elusive responses of wild animals to human activity is important because this may provide information for more proactive conservation planning. In this study, we used camera traps in a field survey technique to investigate the trade-offs between spatial and temporal responses of a mammal community to major human activities in Qinling Mountains, China. We focused on five most abundant mammalian species including giant panda (Ailuropoda melanoleuca), takin (Budorcas taxicolor), wild boar (Sus scrofa), tufted deer (Elaphodus cephalophus), and Chinese goral (Naemorhedus griseus), and examined the drivers of, and the trade-offs between the change of their spatial distributions and daily activity patterns in response to anthropogenic disturbances. We found that in response to human interferences, giant panda and takin mainly changed their distributions, while wild boar, tufted deer and Chinese goral altered their daily activity patterns, indicating the elusive responses of the latter species under anthropogenic stressors. In addition, anthropogenic stressors such as farming and tourism have more profound impacts on mammal communities than previously revealed by species distribution modeling only. For nature reserves that aim to conserve multiple species simultaneously, a more flexible, adaptive management framework is thus needed to capture the trade-offs between multiple species’ spatial and temporal responses to anthropogenic disturbance.

     

Asymmetric evolution of egg laying behavior following reciprocal host shifts by a seed-feeding beetle

Colonization of new environments can lead to rapid changes in fitness-related traits. For herbivorous insects, switching to a new host plant can be comparable to invading a new habitat. Behavioral, physiological, and life-history traits commonly vary among insect populations associated with different plants, but how host shifts cause trait divergence is often unclear. We investigated whether experimental host shifts would modify a key insect trait, egg-laying behavior, in a seed beetle. Beetle populations associated long-term with either a small-seeded host (mung bean) or a large-seeded host (cowpea) were switched to each other’s host. After 36–55 generations, we assayed three aspects of oviposition behavior known to differ between the mung bean- and cowpea-adapted populations. Responses to the host shifts were asymmetrical. Females from lines transferred from mung bean to cowpea produced less uniform distributions of eggs among seeds, were more likely to add an egg to an occupied seed, and were more likely to “dump” eggs when seeds were absent. These lines thus converged toward the cowpea-adapted population. In contrast, the reciprocal host shift had no effect; oviposition behavior was unchanged in lines transferred from cowpea to mung bean. We suggest that these results reflect an asymmetry in the fitness consequences of each host shift, which in turn depended on differences in larval competitiveness in the original populations. Interactions among multiple fitness components are likely to make evolutionary responses less predictable in novel environments.     

Evolution of vertebrate immunity

All multicellular organisms protect themselves against pathogens using sophisticated immune defenses. Functionally interconnected humoral and cellular facilities maintain immune homeostasis in the absence of overt infection and regulate the initiation and termination of immune responses directed against pathogens. Immune responses of invertebrates, such as flies, are innate and usually stereotyped; those of vertebrates, encompassing species as diverse as jawless fish and humans, are additionally adaptive, enabling more rapid and efficient immune reactivity upon repeated encounters with a pathogen. Many of the attributes historically defining innate and adaptive immunity are in fact common to both, blurring their functional distinction and emphasizing shared ancestry and co-evolution. These findings provide indications of the evolutionary forces underlying the origin of somatic diversification of antigen receptors and contribute to our understanding of the complex phenotypes of human immune disorders. Moreover, informed by phylogenetic considerations and inspired by improved knowledge of functional networks, new avenues emerge for innovative therapeutic strategies.