A newly discovered role of evolution in previously published consumer–resource dynamics

Consumer–resource interactions are fundamental components of ecological communities. Classic features of consumer–resource models are that temporal dynamics are often cyclic, with a ¼‐period lag between resource and consumer population peaks. However, there are few published empirical examples of this pattern. Here, we show that many published examples of consumer–resource cycling show instead patterns indicating eco‐evolutionary dynamics. When prey evolve along a trade‐off between defence and competitive ability, two‐species consumer–resource cycles become longer and antiphase (half‐period lag, so consumer maxima coincide with minima of the resource species). Using stringent criteria, we identified 21 two‐species consumer–resource time series, published between 1934 and 1997, suitable to investigate for eco‐evolutionary dynamics. We developed a statistical method to probe for a transition from classic to eco‐evolutionary cycles, and find evidence for eco‐evolutionary type cycles in about half of the studies. We show that rapid prey evolution is the most likely explanation for the observed patterns.     

When relative allocation depends on total resource acquisition: implication for the analysis of trade‐offs

A central tenet of evolutionary biology states that life‐history traits are linked via trade‐offs, as classically exemplified by the van Noordwijk and de Jong model. This model, however, assumes that the relative resource allocation to a biological function varies independently of the total resource acquisition. Based on current empirical evidence, we first explored the dependency between the total resource acquisition and the relative resource allocation to reproduction and showed that such dependency is the rule rather than the exception. We then derived the expression of the covariance between traits when the assumption of independence is relaxed and used simulations to quantify the importance of such dependency on the detection of trade‐offs between current reproduction and future survival. We found that the dependency between the total energy acquisition and the relative allocation to reproduction can influence the probability to detect trade‐offs between survival and reproduction. As a general rule, a negative dependency between the total energy acquisition and the relative allocation to reproduction should lead to a higher probability of detecting a trade‐off in species with a fast pace of life, whereas a positive dependency should lead to a higher probability of detecting a trade‐off in species with a slow pace of life. In addition to confirming the importance of resource variation to reveal trade‐offs, our finding demonstrates that the covariance between resource allocation and resource acquisition is generally not null and also plays a fundamental role in the detection of trade‐offs.     

PREDICTING NUCLEAR GENE COALESCENCE FROM MITOCHONDRIAL DATA: THE THREE-TIMES RULE

Abstract.— Coalescence theory predicts when genetic drift at nuclear loci will result in fixation of sequence differences to produce monophyletic gene trees. However, the theory is difficult to apply to particular taxa because it hinges on genetically effective population size, which is generally unknown. Neutral theory also predicts that evolution of monophyly will be four times slower in nuclear than in mitochondrial genes primarily because genetic drift is slower at nuclear loci. Variation in mitochondrial DNA (mtDNA) within and between species has been studied extensively, but can these mtDNA data be used to predict coalescence in nuclear loci? Comparison of neutral theories of coalescence of mitochondrial and nuclear loci suggests a simple rule of thumb. The “three‐times rule” states that, on average, most nuclear loci will be monophyletic when the branch length leading to the mtDNA sequences of a species is three times longer than the average mtDNA sequence diversity observed within that species. A test using mitochondrial and nuclear intron data from seven species of whales and dolphins suggests general agreement with predictions of the three‐times rule. We define the coalescence ratio as the mitochondrial branch length for a species divided by intraspecific mtDNA diversity. We show that species with high coalescence ratios show nuclear monophyly, whereas species with low ratios have polyphyletic nuclear gene trees. As expected, species with intermediate coalescence ratios show a variety of patterns. Especially at very high or low coalescence ratios, the three‐times rule predicts nuclear gene patterns that can help detect the action of selection. The three‐times rule may be useful as an empirical benchmark for evaluating evolutionary processes occurring at multiple loci.     

Fluctuating resource availability increases invasibility in microbial microcosms

The fluctuating resource hypothesis (FRH) proposes that fluctuations in resource supply can temporally reduce competitive pressure from resident species, thereby providing ephemeral opportunities for invading species. Although FRH has the potential to integrate many existing hypotheses regarding mechanisms of community invasibility, previous tests and evaluations of FRH were based on single trophic level, did not take the timing effect into account, and had difficulties in distinguishing the effects of resource pulses from other simultaneous processes. Here we test FRH in multi‐trophic aquatic microcosms by creating resource pulses, by controlling resource quantity, propagule supply and pulse recurrence frequency, and by manipulating the timing of pulses relative to the timing of the arrival of new species (i.e. invaders) to local communities. The novelty of our work lies in that we directly manipulate resource pulse timing relative to invader introduction events and thus demonstrate the importance of this timing effect for community invasibility. Our study supports FRH in general: invasion success was positively related to resource pulses, and invaders had strong performance in treatments receiving coincident pulses, although not all invaders gained more benefit when resources were supplied at large‐magnitude than supplied at continuous rates. Since many ecosystems worldwide are experiencing high rates of anthropogenic nutrient input and increasing rates of precipitation, these ecosystems are potentially more fragile and susceptible to invasion. More experiments across multiple ecosystem types are needed to help formulate a general theory of community invasibility.     

Context-dependent defence in terrestrial plants: the effects of light and nutrient availability on plant resistance against herbivory

The context‐dependent defence (CDD) hypothesis predicts that defence levels of plant species against herbivory are not fixed but vary with environmental conditions, in a way that is specific for plant species that share evolutionary adaptations to resource conditions exemplified by similar maximum relative growth rates. More specifically, we expected plants from resource‐poor environments to display high defence levels but not when grown under resource‐rich conditions, whereas the reverse – plants from resource‐rich conditions displaying low defence levels but not when grown under resource‐poor conditions – is not necessarily the case. In this study, we used multiple‐choice bioassays in which leaf discs were fed to larvae of Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae) as an efficient and effective way of indicating plant defence levels. This generalist herbivore was capable of detecting both inter‐ and intraspecific differences in defence among plant species. The CDD was tested by exploring the effects of various experimental resource conditions (light, nutrients) upon the herbivore preferences and by comparing these preferences with the maximum relative growth rate of plant species. The experimental results provide general support for the CDD hypothesis with respect to nutrient‐level variation but the effects were not related to the origin of the plant species tested. Variation in light conditions did not result in consistent effects upon herbivore preferences. The CDD therefore can be formulated more precisely as: defence levels of plant species vary under different environmental conditions but in a way that is specific for plant species that share evolutionary adaptations to similar nutrient conditions. This more precise CDD hypothesis is a useful addition to existing optimal‐defence theory because of its focus on the possible plastic effects of resource conditions upon plant defence levels. This is relevant when designing experimental plant–herbivore studies.     

Body size evolution in insular vertebrates: generality of the island rule

Aim My goals here are to (1) assess the generality of the island rule – the graded trend from gigantism in small species to dwarfism in larger species – for mammals and other terrestrial vertebrates on islands and island‐like ecosystems; (2) explore some related patterns of body size variation in insular vertebrates, in particular variation in body size as a function of island area and isolation; (3) offer causal explanations for these patterns; and (4) identify promising areas for future studies on body size evolution in insular vertebrates. Location Oceanic and near‐shore archipelagos, and island‐like ecosystems world‐wide. Methods Body size measurements of insular vertebrates (non‐volant mammals, bats, birds, snakes and turtles) were obtained from the literature, and then regression analyses were conducted to test whether body size of insular populations varies as a function of body size of the species on the mainland (the island rule) and with characteristics of the islands (i.e. island isolation and area). Results The island rule appears to be a general phenomenon both with mammalian orders (and to some degree within families and particular subfamilies) as well as across the species groups studied, including non‐volant mammals, bats, passerine birds, snakes and turtles. In addition, body size of numerous species in these classes of vertebrates varies significantly with island isolation and island area. Main conclusions The patterns observed here – the island rule and the tendency for body size among populations of particular species to vary with characteristics of the islands – are actually distinct and scale‐dependent phenomena. Patterns within archipelagos reflect the influence of island isolation and area on selective pressures (immigration filters, resource limitation, and intra‐ and interspecific interactions) within particular species. These patterns contribute to variation about the general trend referred to as the island rule, not the signal for that more general, large‐scale pattern. The island rule itself is an emergent pattern resulting from a combination of selective forces whose importance and influence on insular populations vary in a predictable manner along a gradient from relatively small to large species. As a result, body size of insular species tends to converge on a size that is optimal, or fundamental, for a particular bau plan and ecological strategy.     

Species sorting and stoichiometric plasticity control community C:P ratio of first‐order aquatic consumers

Ecological stoichiometry has proven to be invaluable for understanding consumer response to changes in resource quality. Although interactions between trophic levels occur at the community level, most studies focus on single consumer species. In contrast to individual species, communities may deal with trophic mismatch not only through elemental plasticity but also through changes in species composition. Here, we show that a community of first‐order consumers (e.g. zooplankton) is able to adjust its stoichiometry (C:P) in response to experimentally induced changes in resource quality, but only to a limited extent. Furthermore, using the Price equation framework we show the importance of both elemental plasticity and species sorting. These results illustrate the need for a community perspective in ecological stoichiometry, requiring consideration of species‐specific elemental composition, intraspecific elemental plasticity and species turnover.     

The impact of consumer-resource cycles on the coexistence of competing consumers

This article seeks to determine the extent to which endogenous consumer-resource cycles can contribute to the coexistence of competing consumer species. It begins with a numerical analysis of a simple model proposed by Armstrong and McGehee. This model has a single resource and two consumers, one with a linear functional response and one with a saturating response. Coexistence of the two consumer species can occur when the species with a saturating response generates population cycles of the resource, and also has a lower resource requirement for zero population growth. Coexistence can be achieved over a wide range of relative efficiencies of the two consumers provided that the functional response of the saturating consumer reaches its half-saturation value when the resource population is a small fraction of its carrying capacity. In this case, the range of efficiencies allowing coexistence is comparable to that when two competitors have stable dynamics and a high degree of resource partitioning. A variety of modifications of this basic model are analyzed to investigate the consequences for coexistence of different resource growth equations, different functional and numerical response shapes, and other factors. Large differences in functional response shape appear to be the most important factor in producing robust coexistence via resource cycles. If the unstable species has a concave numerical response, this greatly expands the conditions allowing coexistence. If the stable consumer species has a convex (accelerating) functional and/or numerical response, the range of conditions allowing coexistence is also expanded. We argue that large between-species differences in functional response form can often be produced by between-consumer differences in the adaptive adjustments of foraging effort to food density. Consumer-resource cycles can also expand the conditions allowing coexistence when there is resource partitioning, but do so primarily when resource partitioning is relatively slight; this makes the ease of coexistence relatively independent of consumer similarity.     

CONSUMER–RESOURCE INTERACTIONS AND THE EVOLUTION OF MIGRATION

Theoretical studies have demonstrated that selection will favor increased migration when fitnesses vary both temporally and spatially, but it is far from clear how pervasive those theoretical conditions are in nature. Although consumer–resource interactions are omnipresent in nature and can generate spatial and temporal variation, it is unknown even in theory whether these dynamics favor the evolution of migration. We develop a mathematical model to address whether and how migration evolves when variability in fitness is determined at least in part by consumer–resource coevolutionary interactions. Our analyses show that such interactions can drive the evolution of migration in the resource, consumer, or both species and thus supplies a general explanation for the pervasiveness of migration. Over short time scales, we show the direction of change in migration rate is determined primarily by the state of local adaptation of the species involved: rates increase when a species is locally maladapted and decrease when locally adapted. Our results reveal that long‐term evolutionary trends in migration rates can differ dramatically depending on the strength or weakness of interspecific interactions and suggest an explanation for the evolutionary divergence of migration rates among interacting species.     

Ecological principles of species distribution models: the habitat matching rule

Most species distribution models (SDMs) assume that habitats are closed, stable and without competition. In that environmental context, it is ecologically correct to assume that members of a species will be distributed in direct relation to the suitability of the habitat, that is, according to the so‐called habitat matching rule. This paper examines whether it is possible to maintain the assumption of the habitat matching rule in the following circumstances: (1) when habitats are connected and organisms can move between them, (2) when there are disturbances and seasonal cycles that generate instability, and (3) when there is inter‐specific and intra‐specific competition. Here I argue that it is possible as long as the following aspects are taken into account. In open habitats at equilibrium, in which habitat selection and competition operate, the habitat matching rule can be applied in some conditions, while competition tends to homogenize the species distribution in other environmental contexts. In the latter case, two methods can be used to incorporate these effects into SDMs: new parameters can be incorporated into the response functions, or the occurrence of proportions of categories of individuals (adult/young, male/female, or dominant/subordinate species in guilds) can be used instead of the occurrence of organisms. The habitat matching rule is not fulfilled in non‐equilibrium environments. The solution to this problem lies in the design of SDMs with two strategies that depend on scale. Locally, the disequilibrium can be encapsulated using average environmental conditions, with sufficiently large cells (in the case of metapopulations) and/or long enough sampling periods (in the case of seasonal cycles). At coarse scales, the use of presence‐only models can in some cases avoid the destabilizing effect of catastrophic historical processes. The matching law is a strong assumption of SDMs because it is based on population ecology theory and the principle of evolution by natural selection.     

Advantages and disadvantages of interference‐competitive ability and resource‐use efficiency when invading established communities

Invaders into established communities must overcome low resource availability. To establish, invaders must either appropriate resources from existing individuals through interference competition or efficiently use the small amount of resource that remains. Although both strategies may be important, they are rarely considered together and, in particular, resource‐use efficiency is often ignored in systems dominated by interference competition. To identify the traits that confer invasion success, we experimentally invaded resource patches in established communities with multiple species from two functional groups that differ in interference competitive ability and resource‐use efficiency. In contrast to previous assessments, we show that resource‐use efficiency can facilitate invasion in systems dominated by interference competition. Furthermore, large resource requirements can be a liability when establishing because interference competition is inherently costly and so cannot fully compensate for limitations in the primary resource. However, we also show that there is a tradeoff in performance among functional groups between small and large resource gaps. Our results suggest we modify the way we view and manage species invasion in systems dominated by interference competition.     

The founding of Mauritian endemic coffee trees by a synchronous long‐distance dispersal event

The stochastic process of long‐distance dispersal is the exclusive means by which plants colonize oceanic islands. Baker's rule posits that self‐incompatible plant lineages are unlikely to successfully colonize oceanic islands because they must achieve a coordinated long‐distance dispersal of sufficiently numerous individuals to establish an outcrossing founder population. Here, we show for the first time that Mauritian Coffea species are self‐incompatible and thus represent an exception to Baker's rule. The genus Coffea (Rubiaceae) is composed of approximately 124 species with a paleotropical distribution. Phylogenetic evidence strongly supports a single colonization of the oceanic island of Mauritius from either Madagascar or Africa. We employ Bayesian divergence time analyses to show that the colonization of Mauritius was not a recent event. We genotype S‐RNase alleles from Mauritian endemic Coffea, and using S‐allele gene genealogies, we show that the Mauritian allelic diversity is confined to just seven deeply divergent Coffea S‐RNase allelic lineages. Based on these data, we developed an individual‐based model and performed a simulation study to estimate the most likely number of founding individuals involved in the colonization of Mauritius. Our simulations show that to explain the observed S‐RNase allelic diversity, the founding population was likely composed of fewer than 31 seeds that were likely synchronously dispersed from an ancestral mainland species.     

Recombination Rate and AT-content Show Opposite Correlations in Mammalian and Other Animal Genomes

Genomes are often characterized by their genome size, recombination rate and nucleotide content. Negative correlations of recombination rate and AT-content have been reported for selected species. Here we investigate 26 completely sequenced animal genomes with respect to their genomic characteristics. After correcting for phylogenetic correlations we find significant correlations between these characters, showing that these do not evolve independently. The genomes of mammals differ when compared to other animal genomes. Correlations between AT-content and recombination rate are negative, but only for mammals. All other animals show a positive correlation for these characters. These results show that studies on the relationship between genome characteristics using single species might lead to the right conclusion, but cannot be applied as a general rule to all taxonomic groups. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Woody species in resource‐rich microrefugia of granite outcrops display unique functional signatures

Refugia are key environments in biogeography and conservation. Because of their unique eco‐evolutionary formation and functioning, they should display distinct functional trait signatures. However, comparative trait‐based studies of plants in refugia and non‐refugia are lacking. Here, we provide a comparison between resource‐rich (putative microrefugia for species preferring mesic habitats under increasing aridity) and resource‐impoverished woodlands (non‐refugia) around two granite outcrops in south‐western Australia. We measured and compared six functional traits (bark thickness, foliar δ¹³C, foliar C:N, leaf dry matter content, plant height, specific leaf area) in four woody species. We performed multiple‐trait, multiple‐species and single‐trait, within‐species analyses to test whether plants in resource‐rich habitats were functionally distinct and more diverse than those in the surrounding resource‐impoverished woodlands. We found that species in resource‐rich woodlands occupied larger and distinct multiple‐trait functional spaces and showed distinct single‐trait values (for specific leaf area and bark thickness). This suggests that plants in resource‐rich woodlands can deploy unique and more diverse ecological strategies, potentially making these putative microrefugia more resilient to environmental changes. These findings suggest that species in microrefugia may be characterised by unique functional signatures, illustrating the utility of comparative trait‐based approaches to improve understanding of the functioning of refugia.     

Optimizing performance of nonparametric species richness estimators under constrained sampling

Understanding the functional relationship between the sample size and the performance of species richness estimators is necessary to optimize limited sampling resources against estimation error. Nonparametric estimators such as Chao and Jackknife demonstrate strong performances, but consensus is lacking as to which estimator performs better under constrained sampling. We explore a method to improve the estimators under such scenario. The method we propose involves randomly splitting species‐abundance data from a single sample into two equally sized samples, and using an appropriate incidence‐based estimator to estimate richness. To test this method, we assume a lognormal species‐abundance distribution (SAD) with varying coefficients of variation (CV), generate samples using MCMC simulations, and use the expected mean‐squared error as the performance criterion of the estimators. We test this method for Chao, Jackknife, ICE, and ACE estimators. Between abundance‐based estimators with the single sample, and incidence‐based estimators with the split‐in‐two samples, Chao2 performed the best when CV < 0.65, and incidence‐based Jackknife performed the best when CV > 0.65, given that the ratio of sample size to observed species richness is greater than a critical value given by a power function of CV with respect to abundance of the sampled population. The proposed method increases the performance of the estimators substantially and is more effective when more rare species are in an assemblage. We also show that the splitting method works qualitatively similarly well when the SADs are log series, geometric series, and negative binomial. We demonstrate an application of the proposed method by estimating richness of zooplankton communities in samples of ballast water. The proposed splitting method is an alternative to sampling a large number of individuals to increase the accuracy of richness estimations; therefore, it is appropriate for a wide range of resource‐limited sampling scenarios in ecology.     

Toxic phytoplankton as a keystone species in aquatic ecosystems: stable coexistence to biodiversity

The effect of allelochemicals released by toxic species in plankton community is often taken into account to reveal plankton biodiversity. Using a minimal chemostat model we show that the interaction between toxic and non‐toxic phytoplankton species with changing competitive effects among species due to allelopathy helps to promote the stable coexistence of many species on a single resource and hence can solve the paradox of plankton. We emphasize toxic phytoplankton as a keystone species that strongly uncovers its allelochemicals on other non‐toxic phytoplankton and enhances the species persistence and diversity in aquatic ecosystems. In addition, we analyze the consistency of ecosystem functioning and species diversity using a number of approaches, such as sampling hypothesis with selection and complementarity effects, cascading extinction–reinvasion, and examining system dynamics at different enrichment levels and toxicity. Our results suggest that chemostats with one toxic and one or more nontoxic phytoplankton species can be used for the experimental verification of the stable coexistence of many species on a single resource in aquatic ecology.     

A synthesis of subdisciplines: predator–prey interactions, and biodiversity and ecosystem functioning

The last 15 years has seen parallel surges of interest in two research areas that have rarely intersected: biodiversity and ecosystem functioning (BEF), and multispecies predator–prey interactions (PPI). Research addressing role of biodiversity in ecosystem functioning has focused primarily on single trophic‐level systems, emphasizing additive effects of diversity that manifest through resource partitioning and the sampling effect. Conversely, research addressing predator–prey interactions has focused on two trophic‐level systems, emphasizing indirect and non‐additive interactions among species. Here, we use a suite of consumer‐resource models to organize and synthesize the ways in which consumer species diversity affects the densities of both resources and consumer species. Specifically, we consider sampling effects, resource partitioning, indirect effects caused by intraguild interactions and non‐additive effects. We show that the relationship between consumer diversity and the density of resources and consumer species are broadly similar for systems with one vs. two trophic levels, and that indirect and non‐additive interactions generally do little more than modify the impacts of diversity established by the sampling effect and resource partitioning. The broad similarities between systems with one vs. two trophic levels argue for greater communication between researchers studying BEF, and researchers studying multispecies PPI.     

Delayed feedback and multiple attractors in a host–parasitoid system

 Continuous-time, age structured, host–parasitoid models exhibit three types of cyclic dynamics: Lotka–Volterra-like consumer-resource cycles, discrete generation cycles, and “delayed feedback cycles” that occur if the gain to the parasitoid population (defined by the number of new female parasitoid offspring produced per host attacked) increases with the age of the host attacked. The delayed feedback comes about in the following way: an increase in the instantaneous density of searching female parasitoids increases the mortality rate on younger hosts, which reduces the density of future older and more productive hosts, and hence reduces the future per head recruitment rate of searching female parasitoids. Delayed feedback cycles have previously been found in studies that assume a step-function for the gain function. Here, we formulate a general host–parasitoid model with an arbitrary gain function, and show that stable, delayed feedback cycles are a general phenomenon, occurring with a wide range of gain functions, and strongest when the gain is an accelerating function of host age. We show by examples that locally stable, delayed feedback cycles commonly occur with parameter values that also yield a single, locally stable equilibrium, and hence their occurrence depends on initial conditions. A simplified model reveals that the mechanism responsible for the delayed feedback cycles in our host–parasitoid models is similar to that producing cycles and initial-condition-dependent dynamics in a single species model with age-dependent cannibalism. Received: 24 October 1997 / Revised version: 13 June 1998     

Bergmann′s rule in mammals: a cross‐species interspecific pattern

Although Bergmann’s rule – stating that among closely related species, the bigger ones will inhabit the colder climates/higher latitudes – was formulated for inter‐specific comparisons, most analyses that tested this pattern in mammals were on an intra‐specific level. To date, no large‐scale taxonomy‐driven cross‐species evaluation of the pattern predicted by Bergmann exists. Here we show, in a dataset comprising 3561 mammal species from 26 orders, that while there is no significant correlation between latitude and body mass using conventional methods, this correlation is highly significant when the phylogenetic structure of the dataset is accounted for, thus supporting Bergmann’s claim that the rule only applies to closely related species. Analyses of different subsets indicate that the Bergmann’s rule is evident across a variety of latitude ranges. In many taxonomic subsets, when analysed alone, there is no significant correlation between body mass and latitude. In combination with both the significant relationship in the overall dataset and with results of intra‐specific analyses from the literature, this suggests that Bergmann’s rule describes a fundamental principle within mammals, but that its expression has been modified by a variety of factors during mammalian diversification yet to be resolved.     

Warming at the population level: Effects on age structure,density, and generation cycles

The impact of climate change on strongly age‐structured populations is poorly understood, despite the central role of temperature in determining developmental rates in ectotherms. Here we examine the effect of warming and its interactions with resource availability on the population dynamics of the pyralid moth Plodia interpunctella, populations of which normally show generation cycles, a consequence of strong and asymmetric age‐related competition. Warming by 3°C above the standard culture temperature led to substantial changes in population density, age structure, and population dynamics. Adult populations were some 50% larger in warmed populations, probably because the reduced fecundity associated with warming leads to reduced larval competition, allowing more larvae to develop to adulthood. Warming also interacted with resource availability to alter population dynamics, with the generation cycles typical of this species breaking down in the 30° populations when standard laboratory diet was provided but not when a reduced nutrient poor diet was used. Warming by 6° led to either rapid extinction or the persistence of populations at low densities for the duration of the experiment. We conclude that even moderate warming can have considerable effects on population structure and dynamics, potentially leading to complete changes in dynamics in some cases. These results are particularly relevant given the large number of economically important species that exhibit generation cycling, in many cases arising from similar mechanisms to those operating in P. interpunctella.