Testing for local adaptation and evolutionary potential along altitudinal gradients in rainforest Drosophila: beyond laboratory estimates

Predicting how species will respond to the rapid climatic changes predicted this century is an urgent task. Species distribution models (SDMs) use the current relationship between environmental variation and species’ abundances to predict the effect of future environmental change on their distributions. However, two common assumptions of SDMs are likely to be violated in many cases: (i) that the relationship of environment with abundance or fitness is constant throughout a species’ range and will remain so in future and (ii) that abiotic factors (e.g. temperature, humidity) determine species’ distributions. We test these assumptions by relating field abundance of the rainforest fruit fly Drosophila birchii to ecological change across gradients that include its low and high altitudinal limits. We then test how such ecological variation affects the fitness of 35 D. birchii families transplanted in 591 cages to sites along two altitudinal gradients, to determine whether genetic variation in fitness responses could facilitate future adaptation to environmental change. Overall, field abundance was highest at cooler, high‐altitude sites, and declined towards warmer, low‐altitude sites. By contrast, cage fitness (productivity) increased towards warmer, lower‐altitude sites, suggesting that biotic interactions (absent from cages) drive ecological limits at warmer margins. In addition, the relationship between environmental variation and abundance varied significantly among gradients, indicating divergence in ecological niche across the species’ range. However, there was no evidence for local adaptation within gradients, despite greater productivity of high‐altitude than low‐altitude populations when families were reared under laboratory conditions. Families also responded similarly to transplantation along gradients, providing no evidence for fitness trade‐offs that would favour local adaptation. These findings highlight the importance of (i) measuring genetic variation in key traits under ecologically relevant conditions, and (ii) considering the effect of biotic interactions when predicting species’ responses to environmental change.     

Context-dependent running speed in funnel-web spiders from divergent populations

1.  Locomotor performance can influence individual fitness through several ecological contexts, such as prey capture and predator escape. One means of determining which contexts act as significant selective forces on running speed is to quantify individual speed in each context. The underlying hypothesis is that animals will exhibit their highest speeds in contexts most crucial to fitness.
2.  We measured running speeds in three ecological contexts (prey capture, fleeing predators and territory defence) in lab-reared offspring of the funnel-web spider Agelenopsis aperta collected from two arid grassland and two riparian populations. Arid populations experience little predation pressure, are prey limited, and are highly territorial; riparian populations experience high predation, have high prey availability, and are less territorial in nature.
3.  The offspring of arid individuals exhibited their highest burst speeds in territory defence, and ran more slowly in response to predator threats. The offspring of riparian populations, however, ran fastest when responding to predatory threats and displayed lower velocities in prey capture and territory defence. Thus, our findings support the hypothesis that A. aperta are selected to exhibit their highest speeds in contexts most important to their fitness.
4.  Contextual use of running speed can differ among conspecific populations experiencing differing selective forces on locomotion.     

The guardians of inherited oncogenic vulnerabilities

Similar to seemingly maladaptive genes in general, the persistence of inherited cancer‐causing mutant alleles in populations remains a challenging question for evolutionary biologists. In addition to traditional explanations such as senescence or antagonistic pleiotropy, here we put forward a new hypothesis to explain the retention of oncogenic mutations. We propose that although natural defenses evolve to prevent neoplasm formation and progression thus increasing organismal fitness, they also conceal the effects of cancer‐causing mutant alleles on fitness and concomitantly protect inherited ones from purging by purifying selection. We also argue for the importance of the ecological contexts experienced by individuals and/or species. These contexts determine the locally predominant fitness‐reducing risks, and hence can aid the prediction of how natural selection will influence cancer outcomes.     

Differences in perceived predation risk associated with variation in relative size of extra‐pair and within‐pair offspring

Extra‐pair paternity (EPP) is a widespread phenomenon in birds. Researchers have long hypothesized that EPP must confer a fitness advantage to extra‐pair offspring (EPO), but empirical support for this hypothesis is definitively mixed. This could be because genetic benefits of EPP only exist in a subset of environmental contexts to which a population is exposed. From 2013 to 2015, we manipulated perceived predator density in a population of tree swallows (Tachycineta bicolor) breeding in New York to see whether fitness outcomes of extra‐pair and within‐pair offspring (WPO) varied with predation risk. In nests that had been exposed to predators, EPO were larger, longer‐winged and heavier than WPO. In nonpredator nests, WPO tended to be larger, longer‐winged and heavier than EPO, though the effect was nonsignificant. We found no differences in age, morphology or stress physiology between extra‐pair and within‐pair sires from the same nest, suggesting that additive genetic benefits cannot fully explain the differences in nestling size that we observed. The lack of an effect of predator exposure on survival or glucocorticoid stress physiology of EPO and WPO further suggests that observed size differences do not reflect more general variation in intrinsic genetic quality. Instead, we suggest that size differences may have arisen through differential investment into EPO and WPO by females, perhaps because EPO and WPO represent different reproductive strategies, with each type of nestling conferring a fitness advantage in specific ecological contexts.     

Ellenberg’s water table experiment put to the test: species optima along a hydrological gradient

An important aspect of niche theory is the position of species’ optima along ecological gradients. It is widely believed that a species’ ecological optimum takes its shape only under competitive pressure. The ecological optimum, therefore, is thought to differ from the physiological optimum in the absence of interspecific competition. Ellenberg’s Hohenheim water table experiment has been very influential in this context. However, the water table gradient in Ellenberg’s experiment was produced by varying the soil thickness above the water table, which confounded the potentially disparate impacts of water table depth (WTD) and soil depth on species growth. Accordingly, here we have re-evaluated Ellenberg’s work. Specifically, we tested the hypothesis that physiological and ecological optima are identical and unaffected by interspecific interaction. We used the same six grasses as in Ellenberg’s experiments, but in our mesocosms, WTD was varied but soil depth kept constant. The design included both an additive component (with/without plant interaction) and a substitutive component (monocultures vs. species mixtures). The results show that the physiological optima along the hydrological gradient varied greatly between species, even in the absence of interspecific interaction. Within species, however, physiological and ecological optima appeared identical in most cases, irrespective of the competition treatment. We conclude that the ‘physiological capacity’ of species largely determines where they are able to persist and that any impact of interspecific interaction is only marginal. These findings are at variance with Ellenberg’s rule, where competition is considered to shift the distribution of a species away from its physiological optimum.     

Ecological correlates of secondary sexual dimorphism in Salix glauca (Salicaceae)

The ecological causation hypothesis for secondary sexual dimorphism was tested in Salix glauca, a dioecious willow shrub. Plants growing in a Colorado Rocky Mountain (USA) krummholz mosaic of mesic and xeric patches were monitored for four consecutive years. Ecological causation is predicated on unique resource demands associated with sexual function. In S. glauca, seeds have twofold higher N and P concentrations compared to pollen. P, but not N, allocation costs differed between sexes at plant and flower scales. Ecological causation also predicts spatial segregation of sexes along underlying habitat gradients. In five populations of S. glauca, sexes displayed significant spatial segregation. The theory also predicts that sexes differ in performance across gradients of environmental stress or resource availability. Consistent with this hypothesis, females had lower drought tolerance than males under years of extreme aridity. Furthermore, over 10 years, annual shoot growth for females was greatest in mesic habitat patches, while males grew at a consistent rate regardless of habitat aridity. Because current shoot growth is correlated with future catkin production, habitat specialization likely provides a fitness payoff in females. Overall, this long-term study provides some of the strongest evidence to date for ecological causation of secondary sexual dimorphism in plants.     

What does the stress‐gradient hypothesis predict? Resolving the discrepancies

In recent years the importance of facilitative interactions in ecological communities is increasingly recognized. This phenomenon has been observed repeatedly, particularly in vegetation communities, in a wide range of environmental conditions. The current hypothesis predicts that the role of facilitation becomes increasingly important in conjunction with increasing stress. Several empirical studies, however, failed to detect such patterns, particularly at the extreme ends of the stress gradients. Herein, we present a conceptual model that may resolve discrepancies between expected and observed and provides a more precise framework of the existing hypotheses. By relaxing two common assumptions commonly used by the stress‐gradient hypothesis (SGH) we are able to demonstrate that under some circumstances the importance of facilitation may be less at the extreme ends of these gradients. Namely, we first re‐emphasize the notion that physiological response is not linear with respect to environmental changes along stress gradients. Second, it is argued that the net outcome of facilitative and competitive interactions is reflected in the fitness of individuals as a product of these two processes, in contrast to the commonly applied assumption of additivity. Accordingly, a synthesis of the concepts of population biology (measures of fitness) and plant physiology (nonlinear responses) with the stress gradient hypothesis while retaining the original simplicity of the SGH model contributes to a better specification of the predictions of the stress‐gradient hypothesis and the resolution of observed contradictions.     

The Effect of Nitrogen and Glyphosate on Survival and Colonisation of Perennial Grass Species in an Agro-Ecosystem: Does the Relative Importance of Survival Decrease with Competitive Ability?

The ecological success of a plant species is typically described by the observed change in plant abundance or cover, but in order to more fully understand the fundamental plant ecological processes, it is necessary to inspect the underlying processes of survival and colonization and how they are affected by environmental conditions. A general ecological hypothesis on the effect of environmental gradients on demographic parameters is proposed and tested. The hypothesis is that decreasing fitness or competitive ability along an environmental gradient is associated with an increasing importance of survival for regulating the abundance of the species. The tested hypothesis is related to both the stress gradient hypothesis and whether the importance of competition increases along productivity gradients. The combined effect of nitrogen and glyphosate on the survival and colonization probability of two perennial grass species, Festuca ovina and Agrostis capillaris, which are known to differ in their responses to both glyphosate and nitrogen treatments, is calculated using pin-point cover data in permanent frames. We found that the relative importance of survival increased with the level of glyphosate for the glyphosate sensitive A. capillaris and decreased for the glyphosate tolerant F. ovina. Likewise, increasing levels of nitrogen increased the importance of survival for the relative nitrophobic F. ovina. Consequently, the proposed hypothesis was corroborated in this specific study. The proposed method will enable predictions of the effects of agricultural practices on community dynamics in a relatively simple setup eliminating the need to quantify all the interaction among the species in the plant community. The method will be immediately useful for the regulation of non-cultivated buffer strips between agricultural fields and semi-natural and natural biotopes such as hedgerows and waterways.     

An examination of genetic variation and selection on condition in Drosophila melanogaster males

According to the genic capture hypothesis, the maintenance of additive genetic variation in fitness-related traits is due to both condition-dependence of these traits and high genetic variation for condition. Evidence supporting this latter assumption is scarce. In this study, we investigated, using hemiclonal analysis, standing genetic variation for condition and relative adult fitness in male Drosophila melanogaster (Meigen) (Diptera: Drosophilidae). The absolute fat and the relative fat content were used as indices of body condition and were measured along with adult relative fitness from males reared in high or low larval densities. The results did not demonstrate genetic variation for condition or adult relative fitness. However, the larval density encountered during development had a strong and significant effect on all traits. Surprisingly, although not significant, negative selection gradients acting on absolute fat and relative fat content were also found in both treatments. These findings challenge one of the main assumptions of the genic capture hypothesis and the use of fat content as an ideal index of condition.     

EXPERIMENTAL STUDIES OF THE EVOLUTIONARY SIGNIFICANCE OF SEXUAL REPRODUCTION II. A TEST OF THE DENSITY-DEPENDENT SELECTION HYPOTHESIS

This study tests the hypothesis that one evolutionary advantage of sexual reproduction is that it produces genetically variable progeny with a density-dependent advantage mediated by resource partitioning or pest pressure. Our experimental approach involved planting separate plots of sexually-derived and asexually-derived tillers of the grass Anthoxanthum odoratum in density gradients at the two natural sites from which the source material was taken. The sexual progeny displayed a significant fitness advantage compared to the asexual progeny. But, in contrast to the expectations of the density-dependent selection hypothesis, the advantage of the sexually produced progeny is most marked at lower densities. Thus, the results of this experiment and our previous report (Antonovics and Ellstrand, 1984) seem to best support the frequency-dependent selection hypothesis for the advantage of sexual reproduction.     

Patterns in the abundance of kangaroo populations in arid Australia are consistent with the exploitation ecosystems hypothesis

The exploitation ecosystems hypothesis (EEH) makes predictions about trophic interactions along gradients of primary productivity. The EEH has been shown to apply to a wide range of terrestrial environments but its applicability to arid environments has received little attention. One reason for this is that arid environments may not satisfy the assumptions of the EEH because dearth of water may limit biological activity in both temporal and spatial contexts. The EEH predicts that herbivore biomass should increase linearly with primary productivity in the absence of predators; but when predators are present herbivore biomass will remain relatively constant due to top down regulation. We tested this prediction in an arid environment using rainfall as a proxy of primary productivity and an index of the abundance of the dominant herbivores (kangaroos Macropus spp.). We compared an index of kangaroo abundance at 18 areas situated along a gradient of mean annual rainfall in areas where a top predator (the dingo Canis lupus dingo) was rare and common. We also explored the relationship between the density of artificial water points (AWPs) and kangaroo abundance to investigate if the resource subsidy provided by AWPs allows kangaroos to persist in high numbers. Consistent with the EEH, kangaroo abundance showed a weak relationship with mean annual rainfall in the presence of dingoes but increased with increasing annual rainfall in the absence of dingoes. The density of AWPs was a poor predictor of kangaroo abundance. Our analysis of macro‐ecological patterns suggests that kangaroo populations are primarily top down regulated in the presence of dingoes, but are bottom up regulated in the absence of dingoes. Our findings provide evidence that top down regulation can prevail over bottom up regulation of herbivore populations in arid ecosystems and highlights the usefulness of the EEH as a predictor of macro‐ecological patterns of species abundance.     

Living on the edge: do central and marginal populations of plants differ in habitat suitability?

The performance of populations at the edge of specie’s distribution range may differ substantially from central populations. Here, we develop a modelling framework to estimate ecological niches (i.e. climatic) of four locally endangered plant species and measure the distance of marginal (geographically) populations to the species’ niche centroid in order to analyse whether marginal populations are outside of the optimal ecological niche of each species. Our results show that for three of the four studied species, which have their populations located at the margins of their distribution ranges, are also at the margins of their climate gradients. These results would support the hypothesis that marginality within the set of habitable conditions (i.e. ecological niche) may represent an important determinant on performance of some plant populations, as well as a plausible explanation to the degree of stagnancy or regression experienced by species in those regions where their populations are at the margin of their ecological niche and/or they are restricted to microrefugia with ecological conditions very different from those around them. Finally, this study aims to be a theoretical base from which to advance on, including other types of factors (e.g. biotic interactions, topography, human influence and population fluctuations through time), which will allow for a better understanding of the complex network of factors that occur in marginal plant populations.     

Departures from neutrality induced by niche and relative fitness differences

Breaking the core assumption of ecological equivalence in Hubbell’s “neutral theory of biodiversity” requires a theory of species differences. In one framework for characterizing differences between competing species, non-neutral interactions are said to involve both niche differences, which promote stable coexistence, and relative fitness differences, which promote competitive exclusion. We include both in a stochastic community model in order to determine if relative fitness differences compensate for changes in community structure and dynamics induced by niche differences, possibly explaining neutral theory’s apparent success. We show that species abundance distributions are sensitive to both niche and relative fitness differences, but that certain combinations of differences result in abundance distributions that are indistinguishable from the neutral case. In contrast, the distribution of species’ lifetimes, or the time between speciation and extinction, differs under all combinations of niche and relative fitness differences. The results from our model experiment are inconsistent with the hypothesis of “emergent neutrality” and support instead a hypothesis that relative fitness differences counteract effects of niche differences on distributions of abundance. However, an even more developed theory of interspecific variation appears necessary to explain the diversity and structure of non-neutral communities.     

Large size in an island-dwelling bird: intraspecific competition and the Dominance Hypothesis

Differences between island‐ and mainland‐dwelling forms provide several classic ecological puzzles. Why, for instance, are island‐dwelling passerine birds consistently larger than their mainland counterparts? We examine the ‘Dominance hypothesis’, based on intraspecific competition, which states that large size in island passerines evolves through selection for success in agonistic encounters. We use the Heron Island population of Capricorn silvereyes (Zosterops lateralis chlorocephalus), a large‐bodied island‐dwelling race of white‐eye (Zosteropidae), to test three assumptions of this hypothesis; that (i) large size is positively associated with high fitness, (ii) large size is associated with dominance, and (iii) the relationship between size and dominance is particularly pronounced under extreme intraspecific competition. Our results supported the first two of these assumptions, but provided mixed evidence on the third. On balance, we suggest that the Dominance Hypothesis is a plausible mechanism for the evolution of large size of island passerines, but urge further empirical tests on the role of intraspecific competition on oceanic islands versus that on mainlands.     

Environment dependence of mutational parameters for viability in Drosophila melanogaster

The genomic rate of mildly deleterious mutations (U) figures prominently in much evolutionary and ecological theory. In Drosophila melanogaster, estimates of U have varied widely, from <0.1 to nearly 1 per zygote. The source of this variation is unknown, but could include differences in the conditions used for assaying fitness traits. We examined how assay conditions affect estimates of the rates and effects of viability-depressing mutations in two sets of lines with accumulated spontaneous mutations on the second chromosome. In each set, the among-line variance in egg-to-adult viability was significantly greater when viability was assayed using a high parental density than when it was assayed using a low density. In contrast, the proportional decline in viability due to new mutations did not differ between densities. Two other manipulations, lowering the temperature and adding ethanol to the medium, had no significant effects on either the mean decline or among-line variance. Cross-environment genetic correlations in viability were generally close to one, implying that most mutations reduced viability in all environments. Using data from the low-density, lower-bound estimates of U approached the classic, high values of Mukai and Ohnishi; at the high density, U estimates were similar to recently reported low values. The difference in estimated mutation rates, taken at face value, would imply that many mutations affected fitness at low density but not at high density, but this is shown to be incompatible with the observed high cross-environment correlations. Possible reasons for this discrepancy are discussed. Regardless of the interpretation, the results show that assay conditions can have a large effect on estimates of mutational parameters for fitness traits.     

FLUCTUATING TEMPERATURE LEADS TO EVOLUTION OF THERMAL GENERALISM AND PREADAPTATION TO NOVEL ENVIRONMENTS

Environmental fluctuations can select for generalism, which is also hypothesized to increase organisms’ ability to invade novel environments. Here, we show that across a range of temperatures, opportunistic bacterial pathogen Serratia marcescens that evolved in fluctuating temperature (daily variation between 24°C and 38°C, mean 31°C) outperforms the strains that evolved in constant temperature (31°C). The growth advantage was also evident in novel environments in the presence of parasitic viruses and predatory protozoans, but less clear in the presence of stressful chemicals. Adaptation to fluctuating temperature also led to reduced virulence in Drosophila melanogaster host, which suggests that generalism can still be costly in terms of reduced fitness in other ecological contexts. While supporting the hypothesis that evolution of generalism is coupled with tolerance to several novel environments, our results also suggest that thermal fluctuations driven by the climate change could affect both species’ invasiveness and virulence.     

Relationships between floristic gradients in a primary succession

Abstract. Correlations between five floristic gradients at small spatial extents (10 - 20 m) and one successional gradient over a larger spatial extent (1.5 km) are analysed. Floristic data (62 taxa) were sampled on five terminal moraines of known age deposited after the ‘Little Ice Age’ (1750–1930). The floristic gradients on the moraine ridges were sampled by two or three transects on each moraine, and the successional gradient by 114 plots on all moraines. The sequential orders of species were determined by constrained and unconstrained Correspondence Analysis. The similarities between species order on the successional gradient and the exposure gradients at the same age were tested against the null hypothesis of no correlation. The null hypothesis was rejected using both Monte Carlo permutation tests and Spearman's rank correlations, except on the oldest moraine. Here a closed canopy has developed, which eliminates the environmental variability associated with ridge morphology. The similarity between the successional gradient and the moraine-ridge gradients is attributed to variation in environmental severity, mainly caused by glacier wind and related factors such as temperature and moisture. Similarity was highest on the moraines in the middle of the glacier foreland, which have many successional stages present and have a relatively exposed relief. The distribution of growth/life-forms along gradients of small spatial extent are comparable to the successional gradient, but lichens, herbs and graminoids differ in their behaviour. The resemblance between species gradients at a small spatial extent and species gradients on a larger spatial extent is interpreted as an ecological self-similar pattern, where young and old substrate are linked to exposed-xeric and protected-mesic habitats, respectively.     

The structure of clines with fitness-dependent dispersal

Spatial models commonly assume that dispersal does not depend on environmental conditions or phenotype. For example, these assumptions underpin explanations for clines on the basis of a trade-off between dispersal and local adaptation. We reexamine clines when an individual's decisions over whether and where to disperse depend on its fitness. We compare fitness-dependent dispersal with cases where dispersal responds to juvenile survivorship only. Clines are steeper the more responsive dispersal is to environmental conditions for all dispersal behaviors that we consider. Clines eventually become stepped as the responsiveness of dispersal to environmental conditions is increased for half of the dispersal behaviors we consider, but smooth clines are maintained for the remaining cases. Smooth clines are maintained by the biased movement of individuals out of the hybrid zone when individuals move directionally in response to gradients in juvenile survivorship, which is a different mechanism to that maintaining smooth clines in classic cline theory.     

Plastic and constant developmental traits contribute to adaptive differences in co-occurring Polygonum species

Adaptive differences among species are often thought to result from developmentally constant trait differences that enhance fitness in alternative environments. Species differences in patterns of individual phenotypic plasticity can also have ecological consequences. Indeed, functionally related constant and plastic traits may interact to determine the phenotype's adaptive value in particular conditions. We compared juvenile shade avoidance traits (height and its components, internode length and node number) across two field density treatments in Polygonumpersicaria and P. hydropiper, annual plant species that co‐occur in pastures comprised of a mosaic of plant densities. We used selection analyses to test trait contributions to fitness in alternative density treatments. Seedlings of both species expressed plasticity for internode elongation in response to density; P. persicaria plants increased internode length and consequently height significantly more in high density than did those of P. hydropiper. As predicted by the shade avoidance hypothesis, increased height was adaptive for both species in high density stands, so P. persicaria plants had higher fitness in this environment. By contrast, node numbers were relatively constant across density treatments in both species: P. hydropiper seedlings consistently produced more nodes than did those of P. persicaria. This constant trait difference contributed to P. hydropiper's greater relative fitness at low density, where more nodes and hence leaves enable plants to better exploit available light. Differences between species in these juvenile shade‐avoidance traits did not result from the evolutionary constraints of lack of heritable variation or costs of plasticity. We discuss how these interspecific trait differences may have been generated by divergent selective histories resulting from differences in herbivore resistance. These results illustrate how adaptive differences in both plastic and constantly expressed traits may jointly contribute to ecological distribution, including coexistence in patchy habitats.     

Symmetric competition as a general model for single-species adaptive dynamics

Adaptive dynamics is a widely used framework for modeling long-term evolution of continuous phenotypes. It is based on invasion fitness functions, which determine selection gradients and the canonical equation of adaptive dynamics. Even though the derivation of the adaptive dynamics from a given invasion fitness function is general and model-independent, the derivation of the invasion fitness function itself requires specification of an underlying ecological model. Therefore, evolutionary insights gained from adaptive dynamics models are generally model-dependent. Logistic models for symmetric, frequency-dependent competition are widely used in this context. Such models have the property that the selection gradients derived from them are gradients of scalar functions, which reflects a certain gradient property of the corresponding invasion fitness function. We show that any adaptive dynamics model that is based on an invasion fitness functions with this gradient property can be transformed into a generalized symmetric competition model. This provides a precise delineation of the generality of results derived from competition models. Roughly speaking, to understand the adaptive dynamics of the class of models satisfying a certain gradient condition, one only needs a complete understanding of the adaptive dynamics of symmetric, frequency-dependent competition. We show how this result can be applied to number of basic issues in evolutionary theory.