Intraspecific genetic variation and competition interact to influence niche expansion

Theory and empirical evidence show that intraspecific competition can drive selection favouring the use of novel resources (i.e. niche expansion). The evolutionary response to such selection depends on genetic variation for resource use. However, while genetic variation might facilitate niche expansion, genetically diverse groups may also experience weaker competition, reducing density-dependent selection on resource use. Therefore, genetic variation for fitness on different resources could directly facilitate, or indirectly retard, niche expansion. To test these alternatives, we factorially manipulated both the degree of genetic variation and population density in flour beetles (Tribolium castaneum) exposed to both novel and familiar food resources. Using stable carbon isotope analysis, we measured temporal change and individual variation in beetle diet across eight generations. Intraspecific competition and genetic variation acted on different components of niche evolution: competition facilitated niche expansion, while genetic variation increased individual variation in niche use. In addition, genetic variation and competition together facilitated niche expansion, but all these impacts were temporally variable. Thus, we show that the interaction between genetic variation and competition can also determine niche evolution at different time scales.     

Intraspecific competition reduces niche width in experimental populations

Intraspecific competition is believed to drive niche expansion, because otherwise suboptimal resources can provide a refuge from competition for preferred resources. Competitive niche expansion is well supported by empirical observations, experiments, and theory, and is often invoked to explain phenotypic diversification within populations, some forms of speciation, and adaptive radiation. However, some foraging models predict the opposite outcome, and it therefore remains unclear whether competition will promote or inhibit niche expansion. We conducted experiments to test whether competition changes the fitness landscape to favor niche expansion, and if competition indeed drives niche expansion as expected. Using Tribolium castaneum flour beetles fed either wheat (their ancestral resource), corn (a novel resource) or mixtures of both resources, we show that fitness is maximized on a mixed diet. Next, we show that at higher population density, the optimal diet shifts toward greater use of corn, favoring niche expansion. In stark contrast, when beetles were given a choice of resources, we found that competition caused niche contraction onto the ancestral resource. This presents a puzzling mismatch between how competition alters the fitness landscape, versus competition's effects on resource use. We discuss several explanations for this mismatch, highlighting potential reasons why optimality models might be misleading.     

Testing the niche variation hypothesis with a measure of body condition

Individual variation and fitness are cornerstones of evolution by natural selection. The niche variation hypothesis (NVH) posits that when interspecific competition is relaxed, intraspecific competition should drive niche expansion by selection favoring use of novel resources and that among‐individual variation should confer a selective advantage. Population‐level niche expansion could be achieved by all individuals using all available resources, or by each individual using a unique combination of resources, thereby increasing among‐individual dietary niche variation. Although individual variation can lead to species‐level evolutionary and ecological change, observed variation does not ensure a beneficial outcome. We used carbon and nitrogen stable isotope analysis of claw keratin and a Bayesian stable isotope mixing model to estimate the summer (July–September) assimilated diet of individual female black Ursus americanus and brown U. arctos bears. We quantified variation in dietary niche in both populations, and assessed diet relative to percentage body fat. We hypothesized that if the NVH held, percentage body fat would be similar for individuals of the same species across much of the dietary range of observed proportional salmon contributions to individual bear diets. Although we found greater differences in dietary niches between than within species, we observed greater among‐individual dietary variation in the brown bear population. Moreover, we found that within each species individual female bears achieved similar ranges of percentage body fat at various levels of salmon in the diet. Our results provide support for the NVH. Linking individual dietary niches to measures of physiological condition related to fitness can offer new insights into eco‐evolutionary processes related to food resource use.     

Novel tri‐isotope ellipsoid approach reveals dietary variation in sympatric predators

Sympatric species may partition resources to reduce competition and facilitate co‐existence. While spatial variation and specialization in feeding strategies may be prevalent among large marine predators, studies have focussed on sharks, birds, and marine mammals. We consider for the first time the isotopic niche partitioning of co‐occurring, teleost reef predators spanning multiple families. Using a novel tri‐isotope ellipsoid approach, we investigate the feeding strategies of seven of these species across an atoll seascape in the Maldives. We demonstrate substantial spatial variation in resource use of all predator populations. Furthermore, within each area, there was evidence of intraspecific variation in feeding behaviors that could not wholly be attributed to individual body size. Assessing species at the population level will mask these intraspecific differences in resource use. Knowledge of resource use is important for predicting how species will respond to environmental change and spatial variation should be considered when investigating trophic diversity.     

Between‐individual variation drives the seasonal dynamics in the trophic niche of a Neotropical marsupial

The dynamics of population niches result from the variation in resource use within individuals and also from the variation between individuals. The prevalence of one mechanism or the other leads to competing hypotheses about the major mechanisms underlying the empirical observations of the contraction/expansion dynamics of the trophic niche in natural populations. In this study, we investigated how within‐ and between‐individual variation in resource use shapes the food niche dynamics of the woolly mouse opossum, Marmosa paraguayana (Didelphimorphia: Didelphidae), in a remnant of the highly seasonal Cerrado in south‐eastern Brazil. To do so, we analysed the faecal samples of live‐trapped individuals to determine their diets within the wet and dry seasons. In addition to a seasonal shift in the composition of the diet, the population trophic niche was significantly wider during the dry season than the wet season. This expansion resulted from larger between‐individual variation in the dry season that was not related to sex preferences, whereas the individual niche widths did not significantly increase from the wet to the dry seasons. Our findings add to the growing list of animal populations that show individual‐level variation in resource use. Furthermore, these results represent a pattern of individual‐level response to seasonal changes that is different from patterns reported for other organisms. We suggest that a pathway to build more realistic foraging models and produce more accurate predictions on population and community dynamics is to consider between‐individual variation and short‐term niche dynamics.     

Seasonal population and individual niche dynamics in a tetra fish in the Pantanal wetlands

In seasonal tropical regions, rainfall and/or temporary floods during the wet season generally increase the abundance and diversity of food resources to many consumers as compared to the dry season. Therefore, seasonality can affect intraspecific competition and ecological opportunity, which are two important ecological mechanisms underlying population and individual niche variations. Here, we took advantage of the strong seasonality in the Pantanal wetlands to investigate how within‐ and between‐individual diet variations relate to seasonal population niche dynamics of the tetra fish Astyanax lacustris. We quantified dietary niche using gut contents and stable isotopes. Tetras had higher gut fullness and better body condition in the wet season, suggesting that competition is more intense in the dry season. The population niche was broader in the wet season due to an increase in diet divergence between individuals, in spite of potential stronger competition in the dry season. We posit that low ecological opportunity in the dry season limits the diversifying effect of intraspecific competition, constraining population niche expansion. Our results add new insights on how seasonality affects population and individual diets, indicating that intraspecific competition and ecological opportunity interact to determine temporal niche variations in seasonal environments.     

Beyond ecological opportunity: Prey diversity rather than abundance shapes predator niche variation

1. Ecological opportunity (i.e. the diversity of available resources) has a pivotal role in shaping niche variation and trophic specialisation of animals. However, ecological opportunity can be described with regard to both diversity and abundance of resources. The degree to which these two components contribute to niche variation remains unexplored.
2. To address this, we used an extensive dataset on fish diet and benthic invertebrate diversity and density from 73 sampling events in three Norwegian rivers in order to explore realised trophic niches and the response of dietary niche variation along gradients of resource diversity (potential trophic niches), resource density (as a proxy of resource abundance) and fish density (as a proxy of inter‐ and intra‐specific competition) in a freshwater top predator (the brown trout, Salmo trutta L.).
3. Linear models indicated that individual and population niche variation increased with increasing ecological opportunity in terms of prey diversity. However, no simple cause‐and‐effect associations between niche indices and prey abundance were found. Our multiple regression analyses indicated that the abundance of certain resources (e.g. Chironomidae) can interact with prey diversity to determine individual and population realised trophic niches. Niche variation (within‐individual component and inter‐individual diet variation) decreased with increasing inter‐ and intra‐specific competition.
4. This study extends prevailing trophic ecology theory by identifying diversity, rather than density, of available prey resources as a primary driver of niche variation in fish of temperate riverine systems with no extensive resource limitation. The study also shows that ecological opportunity may mask the direction of the effect (compression or expansion) of competition on niche variation when food resources are diverse.
5. Our study provides novel empirical insight to the driving forces behind niche variation and reveals that diversity, rather than density, of available prey resources may be a primary driver of niche variation in freshwater fish. Our study supports the view that a broader potential trophic niche promotes broader realised trophic niche variation by individuals, which leads to individual niche diversification by opening access to alternatives resources, resulting in a concomitant rise in the realised trophic niche width of the population.

     

Resource diversity promotes among‐individual diet variation,but not genomic diversity,in lake stickleback

Many generalist species consist of specialised individuals that use different resources. This within‐population niche variation can stabilise population and community dynamics. Consequently, ecologists wish to identify environmental settings that promote such variation. Theory predicts that environments with greater resource diversity favour ecological diversity among consumers (via disruptive selection or plasticity). Alternatively, niche variation might be a side‐effect of neutral genomic diversity in larger populations. We tested these alternatives in a metapopulation of threespine stickleback. Stickleback consume benthic and limnetic invertebrates, focusing on the former in small lakes, the latter in large lakes. Intermediate‐sized lakes support generalist stickleback populations using an even mixture of the two prey types, and exhibit greater among‐individual variation in diet and morphology. In contrast, genomic diversity increases with lake size. Thus, phenotypic diversity and neutral genetic polymorphism are decoupled: trophic diversity being greatest in intermediate‐sized lakes with high resource diversity, whereas neutral genetic diversity is greatest in the largest lakes.     

Pliocene intraspecific divergence and Plio‐Pleistocene range expansions within Picea likiangensis (Lijiang spruce), a dominant forest tree of the Qinghai‐Tibet Plateau

A knowledge of intraspecific divergence and range dynamics of dominant forest trees in response to past geological and climate change is of major importance to an understanding of their recent evolution and demography. Such knowledge is informative of how forests were affected by environmental factors in the past and may provide pointers to their response to future environmental change. However, genetic signatures of such historical events are often weak at individual loci due to large effective population sizes and long generation times of forest trees. This problem can be overcome by analysing genetic variation across multiple loci. We used this approach to examine intraspecific divergence and past range dynamics in the conifer Picea likiangensis, a dominant tree of forests occurring in eastern and southern areas of the Qinghai‐Tibet Plateau (QTP). We sequenced 13 nuclear loci, two mitochondrial DNA regions and three plastid (chloroplast) DNA regions in 177 individuals sampled from 22 natural populations of this species, and tested the hypothesis that its evolutionary history was markedly affected by Pliocene QTP uplifts and Quaternary climatic oscillations. Consistent with the taxonomic delimitation of the three morphologically divergent varieties examined, all individuals clustered into three genetic groups with intervariety admixture detected in regions of geographical overlap. Divergence between varieties was estimated to have occurred within the Pliocene and ecological niche modelling based on 20 ecological variables suggested that niche differentiation was high. Furthermore, modelling of population‐genetic data indicated that two of the varieties (var. rubescens and var. linzhiensis) expanded their population sizes after the largest Quaternary glaciation in the QTP, while expansion of the third variety (var. likiangensis) began prior to this, probably following the Pliocene QTP uplift. These findings point to the importance of geological and climatic changes during the Pliocene and Pleistocene as causes of intraspecific diversification and range shifts of dominant tree species in the QTP biodiversity hot spot region.     

Complex interactions between components of individual prey specialization affect mechanisms of niche variation in a grasshopper-hunting wasp

1.?Individual foraging behaviour defines the use of resources by a given population and its variation in different ways such as, for example, unpredictable interactions between taxon-biased and size-biased selection. Here we investigated how the environmental availability of prey and individual specialization, for both prey taxa and prey size, shape niche variation across generations in the grasshopper-hunting digger wasp Stizus continuus. 2.?The population of S.?continuus expressed selective predation, females mainly hunting species encountered on large bushes; diet changed across generations, due more to size increase in potential prey than to changes in the orthopteran community. 3.?Individual females of both generations weakly overlapped the size and taxa of prey, and the niche width of the second generation increased for both prey size and taxa. 4.?The greater variance in prey size in the environment accounted for the enlarged prey size niche of the second generation, but the load-lifting constraints of the wasps maintained individual prey size specialization constant. In contrast, the enlarged prey taxon niche paralleled a smaller overlap of diets between wasps in the second generation. 5.?Increased niche width in the S.?continuus population was thus achieved in two ways. Regarding prey size, all individuals shifted towards the use of the full set of available resources (parallel release). For prey taxa, according to the classical niche variation hypothesis, individuals diverged to minimize resource use overlap and perhaps intraspecific competition. These two mechanisms were observed for the first time simultaneously in a single predator population.     

Consequences of intraspecific niche variation: phenotypic similarity increases competition among recently metamorphosed frogs

Phenotype is often correlated with resource use, which suggests that as phenotypic variation in a population increases, intraspecific competition will decrease. However, few studies have experimentally tested the prediction that increased intraspecific phenotypic variation leads to reduced competitive effects (e.g., on growth rate, survival or reproductive rate). We investigated this prediction with two experiments on wood frogs (Rana sylvatica). In the first experiment, we found that a frog’s size was positively correlated with the size of its preferred prey, indicating that the feeding niche of the frogs changed with size. In the second experiment, we used an experimental design in which we held the initial mass of “focal” frogs constant, but varied the initial mass of their competitors. We found a significant quadratic effect of the average mass of competitors: focal frog growth was lowest when raised with similar-sized competitors, and highest when raised with competitors that were larger or smaller. Our results demonstrate that growth rates increase (i.e., competitive intensity decreases) when individuals are less similar to other members of the population and exhibit less overlap in resource use. Thus, changes in the amount of phenotypic variation in a population may ultimately affect population-level processes, such as population growth rate and extinction risk.     

Individual diet specialisation in sparrows is driven by phenotypic plasticity in traits related to trade‐offs in animal performance

Individual diet specialisation (IS) is frequent in many animal taxa and affects population and community dynamics. The niche variation hypothesis (NVH) predicts that broader population niches should exhibit greater IS than populations with narrower niches, and most studies that examine the ecological factors driving IS focus on intraspecific competition. We show that phenotypic plasticity of traits associated with functional trade‐offs is an important, but unrecognised mechanism that promotes and maintains IS. We measured nitrogen isotope (δ¹⁵N) and digestive enzyme plasticity in four populations of sparrows (Zonotrichia capensis) to explore the relationship between IS and digestive plasticity. Our results show that phenotypic plasticity associated with functional trade‐offs is related in a nonlinear fashion with the degree of IS and positively with population niche width. These findings are opposite to the NVH and suggest that among individual differences in diet can be maintained via acclimatisation and not necessarily require a genetic component.     

Effectiveness of size frequency distributions in regulating intraspecific spatial overlap of stream insects

Spatial niche breadth and overlap of size groups of four species of epilithic stream insects were studied to determine if broad size frequency distributions serve to reduce intraspecific competition for space. Mean niche overlap decreased with greater breadth of size frequency distributions for only one species (Baetis intercalaris) and did not vary in relation to population density. Similarly, the ratio of the probabilities of intergroup and intragroup encounter did not vary as a function of the breadth of size frequency distributions. Therefore, it was concluded that changes in size frequency distribution have a minimal effect on intraspecific competition for space among epilithic species. It was suggested that observed size frequency distributions may be more a function of extant environmental conditions (temperature and flow) than of previous or extant intraspecific competition.     

Size and shape changes of Ips typographus L. (Coleoptera: Scolytinae) in relation to population level

1 High intraspecific competition is known to occur during Ips typographus outbreaks, and is thought to be the main factor regulating epidemic populations by affecting beetle population productivity. However, little is known about the consequences of intraspecific competition on population quality during outbreaks, although it could have consequences on beetle population dynamics. 2 Ips typographus morphological variations among localities, years and beetle population levels were investigated in 10 Norway spruce (Picea abies) stands having various beetle damage intensities. Beetle size and shape estimators based on wing length, and using isometric size and log‐shape ratios, were employed. Field‐caught beetles were compared with beetles emerging from controlled breeding at different densities, performed in the laboratory. Beetles from this colony were also used to check the influence of breeding densities on the size estimator. 3 Size variations occurred among localities and years and were consistent with the epidemic or latent status of the beetle populations. Controlled breeding confirmed the negative effect of beetle densities encountered in the field on offspring size. Two hypotheses are formulated to explain this increase of intraspecific competition during an outbreak, but our data support the effect of host quality change between latent and epidemic populations. 4 Shape variations also occurred among localities but were unrelated to beetle population levels. No groups consistent with a geographical structure were found, suggesting low genetic variation for I. typographus populations in France.     

Tree,sex and size: Ecological determinants of male vs. female fecundity in three Fagus sylvatica stands

Interindividual variation in fecundities has major consequences on population evolutionary potential, through genetic drift and selection. Using two spatially explicit mating models that analyse the genotypes of seeds and seedlings, we investigated the variation of male and female fecundities within and among three European beech (Fagus sylvatica) stands situated along an altitudinal gradient. Female and male individual fecundity distributions were both skewed in this monoecious species, and we found a higher variance in female as compared to male fecundities. Both female and male fecundities increased with tree size and decreased with density and competition in the neighbourhood, the details of these effects suggesting sex‐specific strategies to deal with the impact of limited resource on fecundity. The studied populations were functionally male‐biased. Among‐individual variations in functional gender were not driven by tree size but by density and competition in the neighbourhood. Femaleness decreased under limited resource availability, an expected consequence of the higher cost of female reproduction. Considering the variation of gene flow and genetic drift across elevation, our results suggest that the adaptive potential could be enhanced by low genetic drift at low elevation, and by high pollen‐mediated gene flow at high elevation. Finally, this study predicts a more efficient response to selection for traits related to male vs. female fitness, for a given selection intensity.     

Impact of past climatic changes and resource availability on the population demography of three food‐specialist bees

Past climate change is known to have strongly impacted current patterns of genetic variation of animals and plants in Europe. However, ecological factors also have the potential to influence demographic history and thus patterns of genetic variation. In this study, we investigated the impact of past climate, and also the potential impact of host plant species abundance, on intraspecific genetic variation in three codistributed and related specialized solitary bees of the genus Melitta with very similar life history traits and dispersal capacities. We sequenced five independent loci in samples collected from the three species. Our analyses revealed that the species associated with the most abundant host plant species (Melitta leporina) displays unusually high genetic variation, to an extent that is seldom reported in phylogeographic studies of animals and plants. This suggests a potential role of food resource abundance in determining current patterns of genetic variation in specialized herbivorous insects. Patterns of genetic variation in the two other species indicated lower overall levels of diversity, and that M. nigricans could have experienced a recent range expansion. Ecological niche modelling of the three Melitta species and their main host plant species suggested a strong reduction in range size during the last glacial maximum. Comparing observed sequence data with data simulated using spatially explicit models of coalescence suggests that M. leporina recovered a range and population size close to their current levels at the end of the last glaciation, and confirms recent range expansion as the most likely scenario for M. nigricans. Overall, this study illustrates that both demographic history and ecological factors may have contributed to shape current phylogeographic patterns.     

The interaction effect between intraspecific competition and seed quality on the life‐history traits of the seed‐feeding beetle Acanthoscelides macrophthalmus

It has been shown that intraspecific competition and resource quality may affect life‐history traits of insects, such as body size, fecundity, and survival. However, intraspecific competition and resource quality may interact with each other. The study of such interacting effects is crucial for understanding the influence of these ecological variables on the selection of specific life‐history traits. Here, we investigated whether the interaction between intraspecific larval competition and variation in resource quality affects adult emergence and survival, egg size, fecundity, body size, and sexual size dimorphism (SSD) of the seed‐feeding beetle Acanthoscelides macrophthalmus (Schaeffer) (Coleoptera: Chrysomelidae: Bruchinae) when infesting Leucaena leucocephala (Lam.) De Wit (Fabaceae), its host plant. In the laboratory, beetles were reared on seeds that differed in quality (e.g., different hardness, seed size, water content), in the presence or absence of larval competition. Body size and SSD did not differ between treatments (with and without competition), nor were they affected by varying resource quality. Females subjected to competition during the larval stage and females emerging from seeds of higher quality, displayed the highest fecundity. The proportion of emergent adults was higher in the absence of competition. In addition, larger eggs were laid on the low‐quality resource in the absence of competition, showing a trade‐off between egg size and egg number. Adult survival differed among treatments and resource qualities, suggesting a higher investment in adult survival for individuals emerging from seeds of low quality in the presence of competition. Whether changes in specific traits could be selected for in detriment of others will depend on the strength of intraspecific competition, the variation in resource quality, and the plasticity in the life‐history traits investigated. This needs further clarification.     

Patterns of niche filling and expansion across the invaded ranges of an Australian lizard

Studies of realized niche shifts in alien species typically ignore the potential effects of intraspecific niche variation and different invaded‐range environments on niche lability. We incorporate our detailed knowledge of the native‐range source populations and global introduction history of the delicate skink Lampropholis delicata to examine intraspecific variation in realized niche expansion and unfilling, and investigate how alternative niche modelling approaches are affected by that variation. We analyzed the realized niche dynamics of L. delicata using an ordination method, ecological niche models (ENMs), and occurrence records from 1) Australia (native range), 2) New Zealand, 3) Hawaii, 4) the two distinct native‐range clades that were the sources for the New Zealand and Hawaii introductions, and 5) the species’ global range (including Lord Howe Island, Australia). We found a gradient of realized niche change across the invaded ranges of L. delicata: niche stasis on Lord Howe Island, niche unfilling in New Zealand (16%), and niche unfilling (87%) and expansion (14%) in Hawaii. ENMs fitted to native‐range data generally identified suitable climatic conditions at sites where the species has established non‐native populations, whereas ENMs based on native‐range source clades and non‐native populations had lower spatial transferability. Our results suggest that the extent to which realized niches are maintained during invasion does not depend on species‐level traits. When realized niche shifts are predominately due to niche unfilling, fully capturing species’ responses along climatic gradients by basing ENMs on native distributions may be more important for accurate invasion forecasts than incorporating phylogenetic differentiation, or integrating niche changes in the invaded range.     

Does intraspecific competition promote variation? A test via synthesis

Competitive diversification, that is, when increasing intraspecific competition promotes population niche expansion, is commonly invoked in evolutionary studies and currently plays a central role in how we conceptualize the process of adaptive diversification. Despite the frequency with which this idea is cited, the empirical evidence for the process is somewhat limited, and the findings of these studies have yet to be weighed objectively through synthesis. Here, we sought to fill this gap by reviewing the existing literature and collecting the data necessary to assess the evidence for competition as a diversifying force. Additionally, we sought to test a more recent hypothesis, which suggests that competition can act to both promote and inhibit dietary diversification depending on the degree to which a consumer depletes its resources. The surprising result of this synthesis was that increasing competition did not have a mean positive effect on population‐level diet breadth or the degree of individual specialization. Instead, we found that increasing intraspecific competition had a restricting effect on population‐level diet breadth in as many cases as it had a diversifying effect. This wide disparity in the effect of competition on consumer diet variation was negatively related to a metric for consumer resource depletion. Altogether, these findings call into question a long‐standing assumption of basic evolutionary models and lend some support to recent theoretical predictions. Specifically, these findings support the idea that competition is primarily diversifying for species with a small effect (per unit biomass) on their resources and that resource depletion limits the diversifying effect of competition for consumers with larger ecological effects.     

The ecology of individuals: incidence and implications of individual specialization

Most empirical and theoretical studies of resource use and population dynamics treat conspecific individuals as ecologically equivalent. This simplification is only justified if interindividual niche variation is rare, weak, or has a trivial effect on ecological processes. This article reviews the incidence, degree, causes, and implications of individual-level niche variation to challenge these simplifications. Evidence for individual specialization is available for 93 species distributed across a broad range of taxonomic groups. Although few studies have quantified the degree to which individuals are specialized relative to their population, between-individual variation can sometimes comprise the majority of the population's niche width. The degree of individual specialization varies widely among species and among populations, reflecting a diverse array of physiological, behavioral, and ecological mechanisms that can generate intrapopulation variation. Finally, individual specialization has potentially important ecological, evolutionary, and conservation implications. Theory suggests that niche variation facilitates frequency-dependent interactions that can profoundly affect the population's stability, the amount of intraspecific competition, fitness-function shapes, and the population's capacity to diversify and speciate rapidly. Our collection of case studies suggests that individual specialization is a widespread but underappreciated phenomenon that poses many important but unanswered questions.