The repeatability of adaptive radiation during long-term experimental evolution of Escherichia coli in a multiple nutrient environment

Adaptive radiations occur when a species diversifies into different ecological specialists due to competition for resources and trade-offs associated with the specialization. The evolutionary outcome of an instance of adaptive radiation cannot generally be predicted because chance (stochastic events) and necessity (deterministic events) contribute to the evolution of diversity. With increasing contributions of chance, the degree of parallelism among different instances of adaptive radiations and the predictability of an outcome will decrease. To assess the relative contributions of chance and necessity during adaptive radiation, we performed a selection experiment by evolving twelve independent microcosms of Escherichia coli for 1000 generations in an environment that contained two distinct resources. Specialization to either of these resources involves strong trade-offs in the ability to use the other resource. After selection, we measured three phenotypic traits: 1) fitness, 2) mean colony size, and 3) colony size diversity. We used fitness relative to the ancestor as a measure of adaptation to the selective environment; changes in colony size as a measure of the evolution of new resource specialists because colony size has been shown to correlate with resource specialization; and colony size diversity as a measure of the evolved ecological diversity. Resource competition led to the rapid evolution of phenotypic diversity within microcosms. Measurements of fitness, colony size, and colony size diversity within and among microcosms showed that the repeatability of adaptive radiation was high, despite the evolution of genetic variation within microcosms. Consistent with the observation of parallel evolution, we show that the relative contributions of chance are far smaller and less important than effects due to adaptation for the traits investigated. The two-resource environment imposed similar selection pressures in independent populations and promoted parallel phenotypic adaptive radiations in all independently evolved microcosms.     

THE DUAL BENEFITS OF APOSEMATISM: PREDATOR AVOIDANCE AND ENHANCED RESOURCE COLLECTION

Theories of aposematism often focus on the idea that warning displays evolve because they work as effective signals to predators. Here, we argue that aposematism may instead evolve because, by enhancing protection, it enables animals to become more exposed and thereby gain resource‐gathering benefits, for example, through a wider foraging niche. Frequency‐dependent barriers (caused by enhanced conspicuousness relative to other prey and low levels of predator education) are generally assumed to make the evolution of aposematism particularly challenging. Using a deterministic, evolutionary model we show that aposematic display could evolve relatively easily if it enabled prey to move more freely around their environments, or become exposed in some other manner that provides fitness benefits unrelated to predation risk. Furthermore, the model shows that the traits of aposematic conspicuousness and behavior which lead to raised exposure positively affect each other, so that the optimal level of both tends to increase when the traits exist together, compared to when they exist in isolation. We discuss the ecological and evolutionary consequences of aposematism. One conclusion is that aposematism could be a key evolutionary innovation, because by widening habitat use it may promote adaptive radiation as a byproduct of enhanced ecological opportunity.     

Ecology and macroevolution – evolutionary niche monopolisation as a mechanisms of niche conservatism

Explaining macroevolution from microevolution is a key issue in contemporary evolutionary theory. A recurrent macroevolutionary pattern is that some niche‐related traits consistently evolve slower than others, so called niche conservatism. Despite a growing amount of data, the underlying evolutionary processes are not fully understood. I here analyse adaptive radiations in an individual‐based eco‐evolutionary model. I find a coevolutionary mechanism – evolutionary niche monopolisation – as a possibly important generator of niche conservatism. A single lineage of a radiating clade can monopolise, and later diversify within, a substantial part of the available niche space – much larger than what can be explained by limiting similarity. This leads to niche conservatism, since no species evolves into or out of the monopolised region. The region can in this sense also be described as an adaptive zone. The model indicates that evolutionary niche monopolisation is operative in a large part of parameter space, underlining its possible importance. The mechanism is driven by competitive interactions and differences in niche widths in alternative niche dimensions. I discuss plausible examples of evolutionary niche monopolisation in well‐studied natural systems.     

Rapid lineage accumulation in a non-adaptive radiation: phylogenetic analysis of diversification rates in eastern North American woodland salamanders (Plethodontidae: Plethodon)

Adaptive radiations have served as model systems for quantifying the build-up of species richness. Few studies have quantified the tempo of diversification in species-rich clades that contain negligible adaptive disparity, making the macroevolutionary consequences of different modes of evolutionary radiation difficult to assess. We use mitochondrial-DNA sequence data and recently developed phylogenetic methodologies to explore the tempo of diversification of eastern North American Plethodon, a species-rich clade of woodland salamanders exhibiting only limited phenotypic disparity. Lineage-through-time analysis reveals a high rate of lineage accumulation, 0.8 species per million years, occurring 11-8 million years ago in the P. glutinosus species group, followed by decreasing rates. This high rate of lineage accumulation is exceptional, comparable to the most rapid of adaptive radiations. In contrast to classic models of adaptive radiation where ecological niche divergence is linked to the origin of species, we propose that phylogenetic niche conservatism contributes to the rapid accumulation of P. glutinosus-group lineages by promoting vicariant isolation and multiplication of species across a spatially and temporally fluctuating environment. These closely related and ecologically similar lineages persist through long-periods of evolutionary time and form strong barriers to the geographic spread of their neighbours, producing a subsequent decline in lineage accumulation. Rapid diversification among lineages exhibiting long-term maintenance of their bioclimatic niche requirements is an under-appreciated phenomenon driving the build-up of species richness.     

Evolution to alternative levels of stable diversity leaves areas of niche space unexplored

One of the oldest and most persistent questions in ecology and evolution is whether natural communities tend to evolve toward saturation and maximal diversity. Robert MacArthur’s classical theory of niche packing and the theory of adaptive radiations both imply that populations will diversify and fully partition any available niche space. However, the saturation of natural populations is still very much an open area of debate and investigation. Additionally, recent evolutionary theory suggests the existence of alternative evolutionary stable states (ESSs), which implies that some stable communities may not be fully saturated. Using models with classical Lotka-Volterra ecological dynamics and three formulations of evolutionary dynamics (a model using adaptive dynamics, an individual-based model, and a partial differential equation model), we show that following an adaptive radiation, communities can often get stuck in low diversity states when limited by mutations of small phenotypic effect. These low diversity metastable states can also be maintained by limited resources and finite population sizes. When small mutations and finite populations are considered together, it is clear that despite the presence of higher-diversity stable states, natural populations are likely not fully saturating their environment and leaving potential niche space unfilled. Additionally, within-species variation can further reduce community diversity from levels predicted by models that assume species-level homogeneity.     

Reconstructing the evolution of birds on islands: 100 years of research

Birds, especially those on islands, have contributed disproportionately to the development of theories that explain the origin and maintenance of organic diversity. This essay surveys the major ideas of how bird species are thought to evolve, speciate and multiply in adaptive radiations on islands. I begin with the nineteenth century view that speciation is the result of natural selection slowly causing divergence of geographically separated populations. I then trace the course of discovery and deeper understanding during the twentieth century, from the influence of Mendelian genetics at the beginning to the modern, molecular era at the end. The dominant and pivotal evolutionary question has been how new species are formed. An initial, nearly exclusive, attention to adaptive processes has been replaced by a search for additional reasons for allopatric divergence, coupled with the conditions that permit coexistence in sympatry after allopatric divergence has occurred. Recent studies have shown that pre‐mating barriers to gene exchange caused by natural selection and sexual selection often arise before post‐mating genetic incompatibilities have evolved. Therefore behavioural and ecological factors play a predominant role in this stage of speciation. Imprinting and imprinting‐like processes of early learning contribute to pre‐mating barriers by constraining mate choice. Ecological factors determine coexistence potential and the fates of hybrids. Genetical factors at all stages, from the founding of a new population to the evolution of genetic incompatibilities, are still poorly known. But molecular genetics is now helping us to reconstruct evolutionary history, thereby transforming ideas about systematic relationships, colonization routes and both the tempo and mode of evolution. As patterns of evolution within radiations become better known, more attention needs to be given to the task of explaining the sequential build‐up of avian communities; by evolutionary radiation and additional immigration, offset to some extent by extinction. The new and substantial challenge is to understand evolutionary radiations in relation to changing environments. Until that challenge is met we cannot claim that the problem of explaining adaptive radiations of birds or any other group of organisms is solved.     

Evolution of niche width and adaptive diversification

Theoretical models suggest that resource competition can lead to the adaptive splitting of consumer populations into diverging lineages, that is, to adaptive diversification. In general, diversification is likely if consumers use only a narrow range of resources and thus have a small niche width. Here we use analytical and numerical methods to study the consequences for diversification if the niche width itself evolves. We found that the evolutionary outcome depends on the inherent costs or benefits of widening the niche. If widening the niche did not have costs in terms of overall resource uptake, then the consumer evolved a niche that was wide enough for disruptive selection on the niche position to vanish; adaptive diversification was no longer observed. However, if widening the niche was costly, then the niche widths remained relatively narrow, allowing for adaptive diversification in niche position. Adaptive diversification and speciation resulting from competition for a broadly distributed resource is thus likely if the niche width is fixed and relatively narrow or free to evolve but subject to costs. These results refine the conditions for adaptive diversification due to competition and formulate them in a way that might be more amenable for experimental investigations.     

Climatic Niche Dynamics and Its Role in the Insular Endemism of <Emphasis Type="Italic">Anolis</Emphasis> Lizards

Insular systems are usually characterized by have a high species diversity, endemism, and evolutionary uniqueness. Although ecological and evolutionary factors shaping insular diversity and endemism are relatively well established, there is a little understanding about climatic niche dynamics for many insular adaptive radiations. Here, we evaluate the tempo and mode of climatic niche evolution in an iconic insular radiation of lizards. By using an extensive dataset of phylogenetic and coarse-grain climatic niches, we evaluated phylogenetic niche divergence and niche conservatism across temporal and spatial scales in the Caribbean Anolis lizard radiation. We found several instances of niche shifts during the anole radiation across islands. Many of these niche shifts converged to similar climatic regimes between different islands. Furthermore, we find evidence that single-island endemic species are more limited by low suitability of climatic conditions outside its native islands than oceanic barriers due to the high climatic heterogeneity observed at least between Greater Antillean islands. These results suggest that within-lineage climatic niche conservatism has been prevalent in short time scales and likely played a role driving the exceptional insular endemism observed today.     

Niche occupation limits adaptive radiation in experimental microcosms

Adaptive radiations have played a key role in the evolution of biological diversity. The breadth of adaptive radiation in an invading lineage is likely to be influenced by the availability of ecological niches, which will be determined to some extent by the diversity of the resident community. High resident diversity may result in existing ecological niches being filled, inhibiting subsequent adaptive radiation. Conversely, high resident diversity could result in the creation of novel ecological niches or an increase in within niche competition driving niche partitioning, thus promoting subsequent diversification. We tested the role of resident diversity on adaptive radiations in experimental populations of the bacterium Pseudomonas fluorescens that readily diversify into a range of niche specialists when grown in a heterogeneous environment. We allowed an undiversified strain to invade resident communities that varied in the number of niche specialists. The breadth of adaptive radiation attainable by an invading lineage decreased with increasing niche occupation of the resident community. Our results highlight the importance of niche occupation as a constraint on adaptive radiation.     

Adaptive radiation in microbial microcosms

It has often been argued that evolutionary diversification is the result of divergent natural selection for specialization on alternative resources. I provide a comprehensive review of experiments that examine the ecology and genetics of resource specialization and adaptive radiation in microbial microcosms. In these experiments, resource heterogeneity generates divergent selection for specialization on alternative resources. At a molecular level, the evolution of specialization is generally attributable to mutations that de-regulate the expression of existing biosynthetic and catabolic pathways. Trade-offs are associated with the evolution of resource specialization, but these trade-offs are often not the result of antagonistic pleiotropy. Replicate adaptive radiations result in the evolution of a similar assemblage of specialists, but the genetic basis of specialization differs in replicate radiations. The implications of microbial selection experiments for evolutionary theory are discussed and future directions of research are proposed.     

Trophic specialization influences the rate of environmental niche evolution in damselfishes (Pomacentridae)

The rate of environmental niche evolution describes the capability of species to explore the available environmental space and is known to vary among species owing to lineage-specific factors. Trophic specialization is a main force driving species evolution and is responsible for classical examples of adaptive radiations in fishes. We investigate the effect of trophic specialization on the rate of environmental niche evolution in the damselfish, Pomacentridae, which is an important family of tropical reef fishes. First, phylogenetic niche conservatism is not detected in the family using a standard test of phylogenetic signal, and we demonstrate that the environmental niches of damselfishes that differ in trophic specialization are not equivalent while they still overlap at their mean values. Second, we estimate the relative rates of niche evolution on the phylogenetic tree and show the heterogeneity among rates of environmental niche evolution of the three trophic groups. We suggest that behavioural characteristics related to trophic specialization can constrain the evolution of the environmental niche and lead to conserved niches in specialist lineages. Our results show the extent of influence of several traits on the evolution of the environmental niche and shed new light on the evolution of damselfishes, which is a key lineage in current efforts to conserve biodiversity in coral reefs.     

Tempo and mode of climatic niche evolution in Primates

Climatic niches have increasingly become a nexus in our understanding of a variety of ecological and evolutionary phenomena, from species distributions to latitudinal diversity gradients. Despite the increasing availability of comprehensive datasets on species ranges, phylogenetic histories, and georeferenced environmental conditions, studies on the evolution of climate niches have only begun to understand how niches evolve over evolutionary timescales. Here, using primates as a model system, we integrate recently developed phylogenetic comparative methods, species distribution patterns, and climatic data to explore primate climatic niche evolution, both among clades and over time. In general, we found that simple, constant‐rate models provide a poor representation of how climatic niches evolve. For instance, there have been shifts in the rate of climatic niche evolution in several independent clades, particularly in response to the increasingly cooler climates of the past 10 My. Interestingly, rate accelerations greatly outnumbered rate decelerations. These results highlight the importance of considering more realistic evolutionary models that allow for the detection of heterogeneity in the tempo and mode of climatic niche evolution, as well as to infer possible constraining factors for species distributions in geographical space.     

EVOLUTION OF THE STORAGE EFFECT

The storage effect, a mechanism that promotes species coexistence in temporally variable environments, poses a dilemma to evolutionary ecologists. Ecological studies have demonstrated its importance in natural communities, but evolutionary models have predicted that selection either impedes coexistence or diminishes the storage effect if there is coexistence. Here, we develop a lottery model of competition in which two species experience a trade‐off in competitive ability between two types of years. We use an adaptive evolution framework to determine conditions favoring the evolution of the storage effect. Storage evolves via divergence of relative performance in the two environments under a wide range of biologically realistic conditions. It evolves between two initially identical species (or lineages) when the trade‐off in performance is strong enough. It evolves for species having different initial trade‐offs for both weak and strong trade‐offs. Our simple 2‐species‐2‐environment scenario can be extended to multiple species and environmental conditions. Results indicate that the storage effect should evolve in a broad range of situations that involve a trade‐off in competitive ability among years, and are consistent with empirical observations. The findings show that storage can evolve in a manner and under conditions similar to other types of resource partitioning.     

Niche construction,human behavior,and the adaptive‐lag hypothesis

Niche construction is the process whereby organisms modify selective environments, thereby affecting evolution. The niche‐construction perspective is particularly relevant to researchers using evolutionary methods to interpret human behavior and society. On the basis of niche‐construction theory, we argue against the hypothesis that modern humans experience an atypically large adaptive lag. We stress that humans construct their world largely to suit themselves and frequently buffer adaptive lag through cultural niche construction. Where they are unable to do that, natural selection of genes rapidly ensues. Our argument has implications for evolutionary psychology and human behavioral ecology, and suggests that the methods of the latter are potentially applicable to all human societies, even postindustrial ones.     

The roles of morphological traits,resource variation and resource partitioning associated with the dietary niche expansion in the fish‐eating bat Myotis pilosus

Niche expansion and shifts are involved in the response and adaptation to environmental changes. However, it is unclear how niche breadth evolves and changes toward higher‐quality resources. Myotis pilosus is both an insectivore and a piscivore. We examined the dietary composition and seasonality in M. pilosus and the closely related Myotis fimbriatus using next‐generation DNA sequencing. We tested whether resource variation or resource partitioning help explain the dietary expansion from insects to fish in M. pilosus. While diet composition and diversity varied significantly between summer and autumn, the proportion of fish‐eating individuals did not significantly change between seasons in M. pilosus. Dietary overlap between M. pilosus and M. fimbriatus during the same seasons was much higher than within individual species across seasons. We recorded a larger body size, hind foot length, and body mass in M. pilosus than in M. fimbriatus and other insectivorous trawling bats from China. Similar morphological differences were found between worldwide fishing bats and nonfishing trawling bats. Our results suggest that variation in insect availability or interspecific competition may not play important roles in the dietary expansion from insects to fish in M. pilosus. Myotis pilosus has morphological advantages that may help it use fish as a diet component. The morphological advantage promoting dietary niche evolution toward higher quality resources may be more important than variation in the original resource and the effects of interspecific competition.     

Is dietary or microhabitat specialization associated with environmental heterogeneity in horned lizards (Phrynosoma)?

Niche breadth is predicted to correlate with environmental heterogeneity, such that generalists will evolve in heterogeneous environments and specialists will evolve in environments that vary less over space and time. We tested the hypothesis that lizards in a heterogeneous environment were generalists compared to lizards in a homogeneous environment. We compared niche breadths of greater short‐horned lizards by quantifying resource selection in terms of two different niche axes, diet (prey items and trophic level), and microhabitat (ground cover and shade cover) between two populations occurring at different elevations. We assessed the heterogeneity of dietary and microhabitat resources within each population's environment by quantifying the availability of prey items, ground cover, and shade cover in each environment. Overall, our results demonstrate that despite differences in resource heterogeneity between elevations, resource selection did not consistently differ between populations. Moreover, environmental heterogeneity was not associated with generalization of resource use. The low‐elevation site had a broader range of available prey items, yet lizards at the high‐elevation site demonstrated more generalization in diet. In contrast, the high‐elevation site had a broader range of available microhabitats, but the lizard populations at both sites were similarly generalized for shade cover selection and were similarly specialized for ground cover selection. Our results demonstrate that environmental heterogeneity of a particular resource does not necessarily predict the degree to which organisms specialize on that resource.     

Strong conservatism of floral morphology during the rapid diversification of the genus Helianthemum

Premise

Divergence of floral morphology and breeding systems are often expected to be linked to angiosperm diversification and environmental niche divergence. However, available evidence for such relationships is not generalizable due to different taxonomic, geographical and time scales. The Palearctic genus Helianthemum shows the highest diversity of the family Cistaceae in terms of breeding systems, floral traits, and environmental conditions as a result of three recent evolutionary radiations since the Late Miocene. Here, we investigated the tempo and mode of evolution of floral morphology in the genus and its link with species diversification and environmental niche divergence.

Methods

We quantified 18 floral traits from 83 taxa and applied phylogenetic comparative methods using a robust phylogenetic framework based on genotyping-by-sequencing data.

Results

We found three different floral morphologies, putatively related to three different breeding systems: type I, characterized by small flowers without herkogamy and low pollen to ovule ratio; type II, represented by large flowers with approach herkogamy and intermediate pollen to ovule ratio; and type III, featured by small flowers with reverse herkogamy and the highest pollen to ovule ratio. Each morphology has been highly conserved across each radiation and has evolved independently of species diversification and ecological niche divergence.

Conclusions

The combined results of trait, niche, and species diversification ultimately recovered a pattern of potentially non-adaptive radiations in Helianthemum and highlight the idea that evolutionary radiations can be decoupled from floral morphology evolution even in lineages that diversified in heterogeneous environments as the Mediterranean Basin.     

Ecological specialization in populations adapted to constant versus heterogeneous environments*

Populations vary in their degree of ecological specialization. An intuitive, but often untested, hypothesis is that populations evolving under greater environmental heterogeneity will evolve to be less specialized. How important is environmental heterogeneity in explaining among‐population variation in specialization? We assessed juvenile viability of 20 Drosophila melanogaster populations evolving under one of four regimes: (1) a salt‐enriched environment, (2) a cadmium‐enriched environment, (3) a temporally varying environment, and (4) a spatially varying environment. Juvenile viability was tested in both the original selective environments and a set of novel environments. In both the original and novel environments, populations from the constant cadmium regime had the lowest average viability and the highest variance in viability across environments but populations from the other three regimes were similar. Our results suggest that variation in specialization among these populations is most simply explained as a pleiotropic by‐product of adaptation to specific environments rather than resulting from a history of exposure to environmental heterogeneity.     

Cooperative personalities and social niche specialization in female meerkats

The social niche specialization hypothesis predicts that group‐living animals should specialize in particular social roles to avoid social conflict, resulting in alternative life‐history strategies for different roles. Social niche specialization, coupled with role‐specific life‐history trade‐offs, should thus generate between‐individual differences in behaviour that persist through time, or distinct personalities, as individuals specialize in particular nonoverlapping social roles. We tested for support for the social niche specialization hypothesis in cooperative personality traits in wild female meerkats (Suricata suricatta) that compete for access to dominant social roles. As cooperation is costly and dominance is acquired by heavier females, we predicted that females that ultimately acquired dominant roles would show noncooperative personality types early in life and before and after role acquisition. Although we found large individual differences in repeatable cooperative behaviours, there was no indication that individuals that ultimately acquired dominance differed from unsuccessful individuals in their cooperative behaviour. Early‐life behaviour did not predict social role acquisition later in life, nor was cooperative behaviour before and after role acquisition correlated in the same individuals. We suggest that female meerkats do not show social niche specialization resulting in cooperative personalities, but that they exhibit an adaptive response in personality at role acquisition.     

The role of climate,water and biotic interactions in shaping biodiversity patterns in arid environments across spatial scales

Aim

Desert ecosystems, with their harsh environmental conditions, hold the key to understanding the responses of biodiversity to climate change. As desert community structure is influenced by processes acting at different spatial scales, studies combining multiple scales are essential for understanding the conservation requirements of desert biota. We investigated the role of environmental variables and biotic interactions in shaping broad and fine‐scale patterns of diversity and distribution of bats in arid environments to understand how the expansion of nondesert species can affect the long‐term conservation of desert biodiversity.

Location

Levant, Eastern Mediterranean.

Methods

We combine species distribution modelling and niche overlap statistics with a statistical model selection approach to integrate interspecific interactions into broadscale distribution models and fine‐scale analysis of ecological requirements. We focus on competition between desert bats and mesic species that recently expanded their distribution into arid environment following anthropogenic land‐use changes.

Results

We show that both climate and water availability limit bat distributions and diversity across spatial scales. The broadscale distribution of bats was determined by proximity to water and high temperatures, although the latter did not affect the distribution of mesic species. At the fine‐scale, high levels of bat activity and diversity were associated with increased water availability and warmer periods. Desert species were strongly associated with warmer and drier desert types. Range and niche overlap were high among potential competitors, but coexistence was facilitated through fine‐scale spatial partitioning of water resources.

Main conclusions

Adaptations to drier and warmer conditions allow desert‐obligate species to prevail in more arid environments. However, this competitive advantage may disappear as anthropogenic activities encroach further into desert habitats. We conclude that reduced water availability in arid environments under future climate change projections pose a major threat to desert wildlife because it can affect survival and reproductive success and may increase competition over remaining water resources.