Evolution Of Ecological Specialization Research Articles

The evolution of ecological specialization across the range of a broadly distributed marine species.

Ecological specialization is an important engine of evolutionary change and adaptive radiation, but empirical evidence of local adaptation in marine environments is rare, a pattern that has been attributed to the high dispersal ability of marine taxa and limited geographic barriers to gene flow. The broad-nosed pipefish, Syngnathus typhle, is one of the most broadly distributed syngnathid species and shows pronounced variation in cranial morphology across its range, a factor that may contribute to its success in colonizing new environments. We quantified variation in cranial morphology across the species range using geometric morphometrics, and tested for evidence of trophic specialization by comparing individual-level dietary composition with the community of prey available at each site. Although the diets of juvenile pipefish from each site were qualitatively similar, ontogenetic shifts in dietary composition resulted in adult populations with distinctive diets consistent with their divergent cranial morphology. Morphological differences found in nature are maintained under common garden conditions, indicating that trophic specialization in S. typhle is a heritable trait subject to selection. Our data highlight the potential for ecological specialization in response to spatially variable selection pressures in broadly distributed marine species.

Narrow entrance of short-tubed Aloe flowers facilitates pollen transfer on long sunbird bills

Trade-offs are considered a major factor in the evolution of ecological specialization, as organisms can rarely specialize on more than one niche. Here we ask whether flowers can be specialized for more than one pollinator group. We studied an outcrossing plant, Aloe kraussii (Asphodelaceae), whose floral morphology is intermediate between that of exclusively bird- and exclusively insect-pollinated aloes. Previous field experiments showed that bees effectively pollinate A. kraussii; while sunbirds are frequent visitors their effectiveness as pollinators was unknown, especially as their long bills prevent head feathers—the normal location of pollen transfer by birds—from touching A. kraussii's relatively short anthers and stigmas. We tested whether sunbirds can pollinate A. kraussii, and whether this might be facilitated by flowers' narrow corolla opening, which could increase pollen transfer via narrow sunbird bills. Aviary experiments showed that a Malachite sunbird's bill can successfully pick up and deposit A. kraussii pollen, so long-billed sunbirds can be effective pollinators despite the apparent mismatch between bill and corolla length. Flowers with experimentally widened corolla openings experienced lower pollen removal and deposition by sunbirds than unmanipulated flowers with narrow openings. Aloe kraussii's floral morphology therefore enables dual specialization on two divergent pollinator guilds; short corollas facilitate bee pollination by enabling access to nectar, while narrow corolla openings facilitate pollen transfer via sunbird bills.

Differences in learning and memory of host plant features between specialist and generalist phytophagous insects

Insects are able to learn from experience acquired in their natal habitat, thereby obtaining adaptive advantages. However, the acquisition of new information could involve defects in retrieving previously learned information (i.e. forgetting), a process known as retroactive interference, which diminishes learning capacities. In this study, we evaluated the learning capacity and the impact of retroactive interference during host searching by ecological specialist and generalist phytophagous insects. We examined whether the generalist aphid, Myzus persicae s. str., and the tobacco-specialized subspecies, Myzus persicae nicotianae differ in (1) learning capacity, or (2) retroactive interference during host selection, and (3) whether the learning-associated foraging gene (for) is differentially expressed. Differences in learning capacity and retroactive interference were assessed in bioassays using rearing hosts and alternative hosts followed by choices between or transferences to rearing or alternative hosts. During the pre-alighting phase of host searching, the generalist aphid showed attraction to the alternative host after 12 h of experience, while the specialist showed no attraction to the alternative host regardless of the amount of time on the plant. The retroactive interference experiments showed that when aphids were exposed to an alternative host for different periods, odour attraction to the rearing host persisted in the generalist after 72 h of experience on the alternative host, whereas in the specialist the attraction to the rearing host was lost after 12 h of experience on the alternative host. During the post-alighting phase of host searching, both taxa performed better on their rearing hosts, but in the specialist aphid, a short period on the alternative host reversed this behaviour. In addition, the specialist showed lower levels of gene for expression, which could be associated with the differences in learning performance. Herein we present further evidence of differences in learning capacities between a specialist and a generalist aphid, which may influence the process of host searching and evolution of ecological specialization.

The evolution of ecological specialization in southern African ungulates: competition‐ or physical environmental turnover?

Using long‐term diet reconstructions spanning the past one million years, we contrast hypotheses that biotic interactions versus physical environmental changes are primary drivers of evolutionary turnover in mammals. We use stable carbon (δ13C) and oxygen (δ18O) isotope ratios in tooth enamel carbonate to trace herbivore niche shifts through the Late Quaternary Land Mammal Ages (LMAs) of grassland savannas in the South African interior (Cornelian‐1.0 to 0.6 Ma; Florisian‐500 to 10 ka; and Holocene/modern). Data reveal niche separation amongst closely related coeval taxa, and dispersals through time into empty niche spaces following extinctions. This suggests a primary role of competitive exclusion and niche displacement for speciation and extinctions in these early grassland environments. However, niche changes through time show a similar trend in many taxa, entailing increased δ13C (elevated C4 grass consumption) from the Cornelian to the Florisian, and from the Florisian to the Holocene/modern, and elevated δ18O in Holocene/modern taxa that reflect global aridification around the terminal Pleistocene. Commonality in isotopic trends implies universal environmental forcing of ecological, and ultimately macroevolutionary, turnover. Yet some taxa shift from a mixed C3/C4 diet in the Florisian to a near‐pure C3 diet today. Indeed, we find that while δ13C data are normally distributed for Cornelian fossils, non‐normal distributions characterize more recent time intervals. Such distributions are in line with the bimodal distribution of δ13C and diet in contemporary African ungulates. Thus, while environmental forcing did not, by necessity, lead to increases in C4 intake, the results show changes from mixed to more specialized diets. We propose that this niche specialization was a function of long‐term exposure to C4 grasslands, consistent with predictions that relatively high metabolic demands of C4 grazing in subtropical environments forced the differentiation of herbivores into one of two highly specialized feeding niches, i.e. C3 browsing or C4 grazing.

THE FITNESS EFFECT OF MUTATIONS ACROSS ENVIRONMENTS: A SURVEY IN LIGHT OF FITNESS LANDSCAPE MODELS

Abstract The fitness effects of mutations on a given genotype are rarely constant across environments to which this genotype is more or less adapted, that is, between more or less stressful conditions. This can have important implications, especially on the evolution of ecological specialization. Stress is thought to increase the variance of mutations' fitness effects, their average, or the number of expressed mutations. Although empirical evidence is available for these three mechanisms, their relative magnitude is poorly understood. In this paper, we propose a simple approach to discriminate between these mechanisms, using a survey of empirical measures of mutation effects in contrasted environments. This survey, across various species and environments, shows that stress mainly increases the variance of mutations effects on fitness, with a much more limited impact on their average effect or on the number of expressed mutations. This pattern is consistent with a simple model in which fitness is a Gaussian function of phenotypes around an environmentally determined optimum. These results suggest that a simple, mathematically tractable landscape model may not be quantitatively as unrealistic as previously suggested. They also suggest that mutation parameter estimates may be strongly biased when measured in stressful environments.

THE FITNESS EFFECT OF MUTATIONS ACROSS ENVIRONMENTS: A SURVEY IN LIGHT OF FITNESS LANDSCAPE MODELS

The fitness effects of mutations on a given genotype are rarely constant across environments to which this genotype is more or less adapted, that is, between more or less stressful conditions. This can have important implications, especially on the evolution of ecological specialization. Stress is thought to increase the variance of mutations' fitness effects, their average, or the number of expressed mutations. Although empirical evidence is available for these three mechanisms, their relative magnitude is poorly understood. In this paper, we propose a simple approach to discriminate between these mechanisms, using a survey of empirical measures of mutation effects in contrasted environments. This survey, across various species and environments, shows that stress mainly increases the variance of mutations' effects on fitness, with a much more limited impact on their average effect or on the number of expressed mutations. This pattern is consistent with a simple model in which fitness is a Gaussian function of phenotypes around an environmentally determined optimum. These results suggest that a simple, mathematically tractable landscape model may not be quantitatively as unrealistic as previously suggested. They also suggest that mutation parameter estimates may be strongly biased when measured in stressful environments.

TACHINIDAE: Evolution, Behavior, and Ecology

Tachinidae are one of the most diverse and ecologically important families in the order Diptera. As parasitoids, they are important natural enemies in most terrestrial ecological communities, particularly as natural enemies of larval Lepidoptera. Despite their diversity and ecological impact, relatively little is known about the evolution and ecology of tachinids, and what is known tends to be widely dispersed in specialized reports, journals, or texts. In this review we synthesize information on the evolutionary history, behavior, and ecology of tachinids and discuss promising directions for future research involving tachinids. We provide an overview of the phylogenetic history and geographic diversity of tachinids, examine the evolution of oviposition strategies and host associations, review known mechanisms of host location, and discuss recent studies dealing with the ecological interactions between tachinids and their hosts. In doing so, we highlight ways in which investigation of these parasitoids provides insight into such topics as biogeographic patterns of diversity, the evolution of ecological specialization, the tritrophic context of enemy-herbivore interactions, and the role of host location behavior in shaping host range.

COUNTERACTING SELECTIVE REGIMES AND HOST PREFERENCE EVOLUTION IN ECOTYPES OF TWO SPECIES OF WALKING-STICKS

The evolution of ecological specialization has been a central topic in ecology because specialized adaptations to divergent environments can result in reproductive isolation and facilitate speciation. However, the order in which different aspects of habitat adaptation and habitat preference evolve is unclear. Timema walking-stick insects feed and mate on the host plants on which they rest. Previous studies of T. cristinae ecotypes have documented divergent, host-specific selection from visual predators and the evolution of divergent host and mate preferences between populations using different host-plant species (Ceanothus or Adenostoma). Here we present new data that show that T. podura, a nonsister species of T. cristinae, has also formed ecotypes on these host genera and that in both species these ecotypes exhibit adaptive divergence in color-pattern and host preference. Color-pattern morphs exhibit survival trade-offs on different hosts due to differential predation. In contrast, fecundity trade-offs on different hosts do not occur in either species. Thus, host preference in both species has evolved before divergent physiological adaptation but in concert with morphological adaptations. Our results shed light onto which traits are involved in the initial stages of ecological specialization and ecologically based reproductive isolation.

The evolution of a pleiotropic fitness tradeoff in Pseudomonas fluorescens.

The evolution of ecological specialization is expected to carry a cost, due to either antagonistic pleiotropy or mutation accumulation. In general, it has been difficult to distinguish between these two possibilities. Here, we demonstrate that the experimental evolution of niche-specialist genotypes of the bacterium Pseudomonas fluorescens that colonize the air-broth interface of spatially structured microcosms is accompanied by pleiotropic fitness costs in terms of reduced carbon catabolism. Prolonged selection in spatially structured microcosms caused the cost of specialization to decline without loss of the benefits associated with specialization. The decline in the cost of specialization can be explained by either compensatory adaptation within specialist lineages or clonal competition among specialist lineages. These results provide a possible explanation of conflicting accounts for the cost of specialization.

The Genetic Architecture of Ecological Specialization: Correlated Gene Effects on Host Use and Habitat Choice in Pea Aphids

Genetic correlations among phenotypic characters result when two traits are influenced by the same genes or sets of genes. By reducing the degree to which traits in two environments can evolve independently (e.g., Lande 1979; Via and Lande 1985), such correlations are likely to play a central role in both the evolution of ecological specialization and in its link to speciation. For example, negative genetic correlations between fitness traits in different environments (i.e., genetic trade-offs) are thought to influence the evolution of specialization, while positive genetic correlations between performance and characters influencing assortative mating can accelerate the evolution of reproductive isolation between ecologically specialized populations. We first discuss how the genetic architecture of a suite of traits may affect the evolutionary role of genetic correlations among them and review how the mechanisms of correlations can be analyzed using quantitative trait locus (QTL) mapping. We then consider the implications of such data for understanding the evolution of specialization and its link to speciation. We illustrate this approach with a QTL analysis of key characters in two races of pea aphids that are highly specialized on different host plants and partially reproductively isolated. Our results suggest that antagonism among QTL effects on performance in the two environments leads to a genetic trade-off in this system. We also found evidence for parallel QTL effects on host-plant acceptance and fecundity on the accepted host, which could produce assortative mating. These results suggest that the genetic architecture of traits associated with host use may have played a central role in the evolution of specialization and reproductive isolation in pea aphids.

The Genetic Architecture of Ecological Specialization: Correlated Gene Effects on Host Use and Habitat Choice in Pea Aphids

Genetic correlations among phenotypic characters result when two traits are influenced by the same genes or sets of genes. By reducing the degree to which traits in two environments can evolve independently (e.g., Lande 1979; Via and Lande 1985), such correlations are likely to play a central role in both the evolution of ecological specialization and in its link to speciation. For example, negative genetic correlations between fitness traits in different environments (i.e., genetic trade‐offs) are thought to influence the evolution of specialization, while positive genetic correlations between performance and characters influencing assortative mating can accelerate the evolution of reproductive isolation between ecologically specialized populations. We first discuss how the genetic architecture of a suite of traits may affect the evolutionary role of genetic correlations among them and review how the mechanisms of correlations can be analyzed using quantitative trait locus (QTL) mapping. We then consider the implications of such data for understanding the evolution of specialization and its link to speciation. We illustrate this approach with a QTL analysis of key characters in two races of pea aphids that are highly specialized on different host plants and partially reproductively isolated. Our results suggest that antagonism among QTL effects on performance in the two environments leads to a genetic trade‐off in this system. We also found evidence for parallel QTL effects on host‐plant acceptance and fecundity on the accepted host, which could produce assortative mating. These results suggest that the genetic architecture of traits associated with host use may have played a central role in the evolution of specialization and reproductive isolation in pea aphids.

When sources become sinks: migrational meltdown in heterogeneous habitats.

We consider the evolution of ecological specialization in a landscape with two discrete habitat types connected by migration, for example, a plant-insect system with two plant hosts. Using a quantitative genetic approach. we study the joint evolution of a quantitative character determining performance in each habitat together with the changes in the population density. We find that specialization on a single habitat evolves with intermediate migration rates, whereas a generalist species evolves with both very low and very large rates of movement between habitats. There is a threshold at which a small increase in the connectivity of the two habitats will result in dramatic decrease in the total population size and the nearly complete loss of use of one of the two habitats through a process of "migrational meltdown." In some situations, equilibria corresponding to a specialist and a generalist species are simultaneously stable. Analysis of our model also shows cases of hysteresis in which small transient changes in the landscape structure or accidental demographic disturbances have irreversible effects on the evolution of specialization.

WHEN SOURCES BECOME SINKS: MIGRATIONAL MELTDOWN IN HETEROGENEOUS HABITATS

We consider the evolution of ecological specialization in a landscape with two discrete habitat types connected by migration, for example, a plant-insect system with two plant hosts. Using a quantitative genetic approach, we study the joint evolution of a quantitative character determining performance in each habitat together with the changes in the population density. We find that specialization on a single habitat evolves with intermediate migration rates, whereas a generalist species evolves with both very low and very large rates of movement between habitats. There is a threshold at which a small increase in the connectivity of the two habitats will result in dramatic decrease in the total population size and the nearly complete loss of use of one of the two habitats through a process of “migrational meltdown.” In some situations, equilibria corresponding to a specialist and a generalist species are simultaneously stable. Analysis of our model also shows cases of hysteresis in which small transient changes in the landscape structure or accidental demographic disturbances have irreversible effects on the evolution of specialization.Corresponding Editor: M. Whitlock

The Shifting Balance Theory of Evolution

Amitabh Joshi studies and teaches evolutionary genetics and population ecology at the Jawaharlal Nehru Centre for Advanced Scientific Research, Bangalore. His current research interests are in life-history evolution, the evolutionary genetics of biological clocks, the evolution of ecological specialization, and small population and metapopulation dynamics. He also enjoys music (especially traditional qawwali in Braj, Farsi, Punjabi and Urdu), history, philosophy, and reading and writing poetry in Urdu, Hindi and English. The Shifting Balance Theory of Evolution is perhaps the most well-known of Sewall Wright’s contributions to evolutionary biology1. This is probably partly because it is a verbal theory, presented with the aid of heuristic pictures, as opposed to much of Wright’s other work in evolution that tended to be rather mathematical. Moreover, this theory was described in many of the most influential books in evolution (written by Dobzhansky, Simpson, and Waddington), published in the middle of the century, that were read by a large number of biologists. Wright himself returned to this theory repeatedly in papers he published (his last paper in 1988 was on this topic), and was very fond of it. The theory itself has been controversial and confusing to many but has, at the same time, also helped many people to think about the evolutionary process in real populations. Ultimately, perhaps, the shifting balance theory has been not so much a rigorous theory, as a picturesque and thought provoking metaphor that has proven helpful in incorporating a spatial dimension into our thinking on evolution.