The succession of ecological divergence and reproductive isolation in adaptive radiations.

Adaptive radiation is a major source of biodiversity but the way in which known components of ecological opportunity, ecological differentiation, and reproductive isolation underpin such biodiversity patterns remains elusive. Much is known about the evolution of ecological differentiation and reproductive isolation during single speciation events, but exactly how those processes scale up to complete adaptive radiations is less understood. Do we expect complete reproductive barriers between newly formed species before the ecological differentiation continues, or does proper species formation occur much later, long after the ecological diversification? Our goal is to improve our mechanistic understanding of adaptive radiations by analyzing an individual-based model that includes a suite of mechanisms that are known to contribute to biodiversity. The model includes variable biogeographic settings, ecological opportunities, and types of mate choice, which makes several different scenarios of an adaptive radiation possible. We find that evolving clades tend to exploit ecological opportunities early whereas reproductive barriers evolve later, demonstrating a decoupling of ecological differentiation and species formation. In many cases, we also find a long-term trend where assortative mating associated with ecological traits is replaced by sexual selection of neutral display traits as the primary mechanism for reproductive isolation. Our results propose that reticulate phylogenies are likely common and stem from initially low reproductive barriers, rather than the previously suggested idea of repeated hybridization events between well-separated species.

Coevolution, diversification and alternative states in two-trophic communities.

Single-trait eco-evolutionary models of arms races between consumers and their resource species often show inhibition rather than promotion of community diversification. In contrast, modelling arms races involving multiple traits, we found that arms races can promote diversification when trade-off costs among traits make simultaneous investment in multiple traits either more beneficial or more costly. Coevolution between resource and consumer species generates an adaptive landscape for each, with the configuration giving predictable suites of consumer and resource species. Nonetheless, the adaptive landscape contains multiple alternative stable states, and which stable community is reached depends on small stochastic differences occurring along evolutionary pathways. Our results may solve a puzzling conflict between eco-evolutionary theory that predicts community diversification via consumer-resource interactions will be rare, and empirical research that has uncovered real cases. Furthermore, our results suggest that these real cases might be just a subset of alternative stable communities.

Principles of niche expansion.

Niche expansion is attained by adaptations in two generalized phenotypical traits-niche position and niche width. This gives room for a wide range of conceptual ways of niche filling. The niche variation hypothesis reduces the range by predicting that expansion occurs by increasing variation in niche position, which has been debated on empirical and theoretical grounds as also other options seem possible. Here, we propose a general theory of niche expansion. We review empirical data and show with an eco-evolutionary model how resource diversity and a trade-off in resource acquisition steer niche evolution consistent with observations. We show that the range can be reduced to a discrete set of two orthogonal ways of niche filling, through (1) strict phenotypical differentiation in niche position or (2) strict individual generalization. When individual generalization is costly, niche expansion undergoes a shift from (2) to (1) at a point where the resource diversity becomes sufficiently large. Otherwise, niche expansion always follows (2), consistent with earlier results. We show that this either-or response can operate at both evolutionary and short-term time scales. This reduces the principles of niche expansion under environmental change to a notion of orthogonality, dictated by resource diversity and a resource-acquisition trade-off.

The Biogeography of Adaptive Radiations and the Geographic Overlap of Sister Species.

The biogeography of speciation and what can be learned about the past mode of speciation from current biogeography of sister species are recurrent problems in evolution. We used a trait- and individual-based, eco-evolutionary model to simulate adaptive radiations and recorded the geographical overlap of species during and after evolutionary branching (speciation). We compared the spatial overlap among sister species in the fully saturated community with the overlap at the speciation event. The mean geographic overlap at speciation varied continuously from complete (sympatry) to none (allopatry), depending on local and regional environmental heterogeneity and the rate of dispersal. The distribution of overlap was, however, in some cases considerably bimodal. This tendency was most expressed at large values of regional heterogeneity, corresponding to sharp environmental contrasts. The mean geographic overlap also varied during the course of a radiation, sometimes with a consistent negative trend over time. The speciations that resulted in currently observable end community sister species were therefore not an unbiased sample of all speciations throughout the radiation. Postspeciation range shifts (causing increased overlap) occurred most frequently when dispersal was high or when local habitat heterogeneity was low. Our results help us understand how the patterns of geographic mode of speciation emerge. We also show the difficulty in inferring the geographical speciation mode from phylogenies and the biogeography of extant species.

Phenology of two interdependent traits in migratory birds in response to climate change.

In migratory birds, arrival date and hatching date are two key phenological markers that have responded to global warming. A body of knowledge exists relating these traits to evolutionary pressures. In this study, we formalize this knowledge into general mathematical assumptions, and use them in an ecoevolutionary model. In contrast to previous models, this study novelty accounts for both traits-arrival date and hatching date-and the interdependence between them, revealing when one, the other or both will respond to climate. For all models sharing the assumptions, the following phenological responses will occur. First, if the nestling-prey peak is late enough, hatching is synchronous with, and arrival date evolves independently of, prey phenology. Second, when resource availability constrains the length of the pre-laying period, hatching is adaptively asynchronous with prey phenology. Predictions for both traits compare well with empirical observations. In response to advancing prey phenology, arrival date may advance, remain unchanged, or even become delayed; the latter occurring when egg-laying resources are only available relatively late in the season. The model shows that asynchronous hatching and unresponsive arrival date are not sufficient evidence that phenological adaptation is constrained. The work provides a framework for exploring microevolution of interdependent phenological traits.

The role of harvesting in age-structured populations: disentangling dynamic and age truncation effects.

Understanding the processes generating fluctuations of natural populations lies at the very heart of academic ecology. It is also very important for applications such as fisheries management and pest control. We are interested in the effect of harvesting on population fluctuations and for that purpose we develop and analyze an age-structured model where recruitment is a stochastic process and the adult segment of the population is harvested. When a constant annual harvest is taken the coefficient of variation of the adult population increases for most parameter values due to the age truncation effect, i.e. an increased variability in a juvenescent population due to the removal of older individuals. However, if a constant proportion of the adults is harvested the age truncation effect is sometimes counteracted by a stabilizing dynamic effect of harvesting. Depending on parameter values mirroring different life histories, proportional harvest can either increase or decrease the relative fluctuations of an exploited population. When there is a demographic Allee effect the ratio of juveniles to adults may actually decrease with harvesting. We conclude that, depending on life history and harvest strategy, harvesting can either reinforce or dampen population fluctuations due to the relative importance of stabilizing dynamic effects and the age truncation effect. The strength of the latter is highly dependent on the fished population's endogenous, age-structured dynamics. More specifically, we predict that populations with strong and positively autocorrelated dynamics will show stronger age truncation effect, a testable prediction that offers a simple rule-of-thumb assessment of a population's vulnerability to exploitation.

The strength of species interactions modifies population responses to environmental variation in competitive communities.

The life-history parameters of most living organisms are modified by fluctuations in environmental conditions. The impact of environmental autocorrelation on population persistence is well understood in single species systems. However, in multi-species communities the impact of stochasticity is complicated by the possibility of different species having differing intrinsic responses to the environment (environmental correlation). Previous work has shown that whether increasing between-species environmental correlation stabilises population fluctuations or not, depends on an interaction between density-dependence and environmental autocorrelation. Here we derive analytical conditions for how this interaction in turn depends on the strength of interspecific competition. Under relatively weak between-species interactions, increasing environmental autocorrelation always dampens population fluctuations, while increasing autocorrelation destabilises strongly interacting populations. In contrast, under intermediate interaction strengths, increasing autocorrelation destabilises (stabilises) population dynamics when populations respond independently (similarly) to environmental fluctuations. These results apply to a wide range of competitive communities and also have some relevance to consumer-resource systems. The results presented here help us better understand population responses to environmental fluctuations under different conditions.

Primary assembly of soil communities: disentangling the effect of dispersal and local environment.

It has long been recognised that dispersal abilities and environmental factors are important in shaping invertebrate communities, but their relative importance for primary soil community assembly has not yet been disentangled. By studying soil communities along chronosequences on four recently emerged nunataks (ice-free land in glacial areas) in Iceland, we replicated environmental conditions spatially at various geographical distances. This allowed us to determine the underlying factors of primary community assembly with the help of metacommunity theories that predict different levels of dispersal constraints and effects of the local environment. Comparing community assembly of the nunataks with that of non-isolated deglaciated areas indicated that isolation of a few kilometres did not affect the colonisation of the soil invertebrates. When accounting for effects of geographical distances, soil age and plant richness explained a significant part of the variance observed in the distribution of the oribatid mites and collembola communities, respectively. Furthermore, null model analyses revealed less co-occurrence than expected by chance and also convergence in the body size ratio of co-occurring oribatids, which is consistent with species sorting. Geographical distances influenced species composition, indicating that the community is also assembled by dispersal, e.g. mass effect. When all the results are linked together, they demonstrate that local environmental factors are important in structuring the soil community assembly, but are accompanied with effects of dispersal that may "override" the visible effect of the local environment.

The risk of competitive exclusion during evolutionary branching: effects of resource variability, correlation and autocorrelation.

Evolutionary branching has been suggested as a mechanism to explain ecological speciation processes. Recent studies indicate however that demographic stochasticity and environmental fluctuations may prevent branching through stochastic competitive exclusion. Here we extend previous theory in several ways; we use a more mechanistic ecological model, we incorporate environmental fluctuations in a more realistic way and we include environmental autocorrelation in the analysis. We present a single, comprehensible analytical result which summarizes most effects of environmental fluctuations on evolutionary branching driven by resource competition. Corroborating earlier findings, we show that branching may be delayed or impeded if the underlying resources have uncorrelated or negatively correlated responses to environmental fluctuations. There is also a strong impeding effect of positive environmental autocorrelation, which can be related to results from recent experiments on adaptive radiation in bacterial microcosms. In addition, we find that environmental fluctuations can lead to cycles of repeated branching and extinction.

Bet-hedging as an evolutionary game: the trade-off between egg size and number.

Bet-hedging theory addresses how individuals should optimize fitness in varying and unpredictable environments by sacrificing mean fitness to decrease variation in fitness. So far, three main bet-hedging strategies have been described: conservative bet-hedging (play it safe), diversified bet-hedging (don't put all eggs in one basket) and adaptive coin flipping (choose a strategy at random from a fixed distribution). Within this context, we analyse the trade-off between many small eggs (or seeds) and few large, given an unpredictable environment. Our model is an extension of previous models and allows for any combination of the bet-hedging strategies mentioned above. In our individual-based model (accounting for both ecological and evolutionary forces), the optimal bet-hedging strategy is a combination of conservative and diversified bet-hedging and adaptive coin flipping, which means a variation in egg size both within clutches and between years. Hence, we show how phenotypic variation within a population, often assumed to be due to non-adaptive variation, instead can be the result of females having this mixed strategy. Our results provide a new perspective on bet-hedging and stress the importance of extreme events in life history evolution.

Environmental variation in ecological communities and inferences from single-species data.

Data are often collected for a single species within an ecological community, so quantitative tools for drawing inferences about the unobserved portions of the community from single-species data are valuable. In this paper, we present and examine a method for estimating community dimension (the number of strongly interacting species or groups) from time series data on a single species. The dynamics of one species can be strongly affected by environmental stochasticity acting not only on itself, but also on other species with which it interacts. By fully accounting for the effects of stochasticity on populations embedded in a community, our approach gives better estimates of community dimension than commonly used methods. Using a combination of time series data and simulations, we show that failing to properly account for stochasticity when attempting to relate population dynamics to attributes of the community can give misleading information about community dimension.

Biodiversity loss through speciation collapse: Mechanisms, warning signals, and possible rescue.

Speciation is the process that generates biodiversity, but recent empirical findings show that it can also fail, leading to the collapse of two incipient species into one. Here, we elucidate the mechanisms behind speciation collapse using a stochastic individual-based model with explicit genetics. We investigate the impact of two types of environmental disturbance: deteriorated visual conditions, which reduce foraging ability and impede mate choice, and environmental homogenization, which restructures ecological niches. We find that: (1) Species pairs can collapse into a variety of forms including new species pairs, monomorphic or polymorphic generalists, or single specialists. Notably, polymorphic generalist forms may be a transient stage to a monomorphic population; (2) Environmental restoration enables species pairs to reemerge from single generalist forms, but not from single specialist forms; (3) Speciation collapse is up to four orders of magnitude faster than speciation, while the reemergence of species pairs can be as slow as de novo speciation; (4) Although speciation collapse can be predicted from either demographic, phenotypic, or genetic signals, observations of phenotypic changes allow the most general and robust warning signal of speciation collapse. We conclude that factors altering ecological niches can reduce biodiversity by reshaping the ecosystem's evolutionary attractors.

Will sympatric speciation fail due to stochastic competitive exclusion?

Sympatric speciation requires coexistence of the newly formed species. If divergence proceeds by small mutational steps, the new species utilize almost the same resources initially, and full speciation may be impeded by competitive exclusion in stochastic environments. We investigate this primarily ecological problem of sympatric speciation by studying the population dynamics of a diverging asexual population in a fluctuating environment. Correlation between species responses to environmental fluctuation is assumed to decrease with distance in trait space. Rapidly declining correlation in combination with high environmental variability may delay full speciation or even render it impossible. Stochastic extinctions impeding speciation are most likely when correlation decays faster than competition, for example, when demographic stochasticity is strong or when divergence is not accompanied by niche separation, such as in speciation driven entirely by sexual selection. Our general theoretical results show an interesting connection between short-term ecological dynamics and long-term, large-scale evolution.

A theory of stochastic harvesting in stochastic environments.

We investigate how model populations respond to stochastic harvesting in a stochastic environment. In particular, we show that the effects of variable harvesting on the variance in population density and yield depend critically on the autocorrelation of environmental noise and on whether the endogenous dynamics of the population display over- or undercompensation to density. These factors interact in complicated ways; harvesting shifts the slope of the renewal function, and the net effect of this shift will depend on the sign and magnitude of the other influences. For example, when environmental noise exhibits a positive autocorrelation, the relative importance of a variable harvest to the variance in density increases with overcompensation but decreases with undercompensation. For a fixed harvesting level, an increasing level of autocorrelation in environmental noise will decrease the relative variation in population density when overcompensation would otherwise occur. These and other intricate interactions have important ramifications for the interpretation of time series data when no prior knowledge of demographic or environmental details exists. These effects are important whenever the harvesting rate is sufficiently high or variable, conditions likely to occur in many systems, whether the harvesting is caused by commercial exploitation or by any other strong agent of density-independent mortality.

Mutant invasions and adaptive dynamics in variable environments.

The evolution of natural organisms is ultimately driven by the invasion and possible fixation of mutant alleles. The invasion process is highly stochastic, however, and the probability of success is generally low, even for advantageous alleles. Additionally, all organisms live in a stochastic environment, which may have a large influence on what alleles are favorable, but also contributes to the uncertainty of the invasion process. We calculate the invasion probability of a beneficial, mutant allele in a monomorphic, large population subject to stochastic environmental fluctuations, taking into account density- and frequency-dependent selection, stochastic population dynamics and temporal autocorrelation of the environment. We treat both discrete and continuous time population dynamics, and allow for overlapping generations in the continuous time case. The results can be generalized to diploid, sexually reproducing organisms embedded in communities of interacting species. We further use these results to derive an extended canonical equation of adaptive dynamics, predicting the rate of evolutionary change of a heritable trait on long evolutionary time scales.

The origin of polymorphic crypsis in a heterogeneous environment.

Polymorphic crypsis has been observed in several taxa, but has, until now, lacked a firm theoretical understanding. How does a single morph, well camouflaged in one type of habitat, evolve crypsis in another, not isolated, habitat? We here analyze a model of one prey species living in two different habitats connected by passive dispersal. We find that the rate of dispersal, the trade-off between crypticity in the habitats, and the amount of predation determines whether the prey species can become cryptic in two different habitats through evolutionary branching. Intermediate values of all parameters seem to promote evolutionary branching leading to polymorphism, and a more extreme value of one parameter can be balanced by another. Other parameter combinations lead to either a single habitat specialist or an intermediate generalist type, partly cryptic in both habitats. When the predator follows a type III functional response, the parameter space for when the prey will undergo evolutionary branching is remarkably larger than the corresponding parameter space for a type II functional response. Evolutionary branching can occur both at the intermediate generalist strategy, or close to a specialist strategy.

Food web dynamics in correlated and autocorrelated environments.

The densities of populations in a community or food web vary as a consequence of both population interactions and environmental (e.g. weather) fluctuations. Populations often respond to the same kinds of environmental fluctuations, and therefore experience correlated environments. Furthermore, some environmental factors change slowly over time, thereby producing positive environmental autocorrelation. We show that the effects of environmental correlation and autocorrelation on the dynamics of the populations in a food web can be large and unintuitive, but can be understood by analyzing the eigenvectors of the community (system) matrix of interactions among populations. For example, environmental correlation and autocorrelation may either obscure or enhance the cyclic dynamics that generally characterize predator-prey interactions even when there is no direct effect of the environment on how species interact. Thus, understanding the population dynamics of species in a food web requires explicit attention to the correlation structure of environmental factors affecting all species.