Heterogeneous adaptive trajectories of small populations on complex fitness landscapes

Background

Small populations are thought to be adaptively handicapped, not only because they suffer more from deleterious mutations but also because they have limited access to new beneficial mutations, particularly those conferring large benefits.

Methodology/Principal Findings

Here, we test this widely held conjecture using both simulations and experiments with small and large bacterial populations evolving in either a simple or a complex nutrient environment. Consistent with expectations, we find that small populations are adaptively constrained in the simple environment; however, in the complex environment small populations not only follow more heterogeneous adaptive trajectories, but can also attain higher fitness than the large populations. Large populations are constrained to near deterministic fixation of rare large-benefit mutations. While such determinism speeds adaptation on the smooth adaptive landscape represented by the simple environment, it can limit the ability of large populations from effectively exploring the underlying topography of rugged adaptive landscapes characterized by complex environments.

Conclusions

Our results show that adaptive constraints often faced by small populations can be circumvented during evolution on rugged adaptive landscapes.     

Adaptation and constraint in a stickleback radiation

The evolution of threespine sticklebacks in freshwater lakes constitutes a well‐studied example of a phenotypic radiation that has produced numerous instances of parallel evolution, but the exact selective agents that drive these changes are not yet fully understood. We present a comparative study across 74 freshwater populations of threespine stickleback in Norway to test whether evolutionary changes in stickleback morphology are consistent with adaptations to physical parameters such as lake depth, lake area, lake perimeter and shoreline complexity, variables thought to reflect different habitats and feeding niches. Only weak indications of adaptation were found. Instead, populations seem to have diversified in phenotypic directions consistent with allometric scaling relationships. This indicates that evolutionary constraints may have played a role in structuring phenotypic variation across freshwater populations of stickleback. We also tested whether the number of lateral plates evolved in response to lake calcium levels, but found no evidence for this hypothesis.     

Contrasting effects of natural habitat loss on generalist and specialist aphid natural enemies

The greater susceptibility of higher trophic levels to habitat loss has been demonstrated to disrupt important trophic interactions such as consumer control of prey populations. This pattern is predicted to break down for generalist species that can use matrix habitats, yet empirical studies comparing generalist and specialist enemy pressure in response to natural habitat loss are lacking. Here we examined the effects of landscape simplification resulting from habitat conversion to agriculture on nettles, Urtica dioica , their specialized aphid herbivore, Microlophium carnosum , and associated natural enemies that varied broadly in their degree of specialization. Both nettles and their specialized aphid herbivore were significantly more abundant in complex than simple landscapes. Different enemy groups showed contrasting responses. Aphid specialists (parasitic wasps and cecidomyiid midges) reached higher densities in complex than simple landscapes, and this effect was primarily related to shifts in local resource abundance (i.e. nettle aphid densities). In contrast, densities of generalists (coccinellid beetles and spiders) were significantly higher in simple landscapes, presumably due to spillover of generalists from surrounding cropland habitats. Natural enemy-prey ratios did not differ significantly across landscape types for specialist groups but were significantly higher in simple than complex landscapes for generalist groups, suggesting that enemy pressure on nettle aphids likely increases with landscape simplification. This was supported by our finding that aphid population growth rates were lower in simple than complex landscapes, and declined significantly with increasing coccinellid densities. Thus, in marked contrast to previous work, our results suggest that natural habitat loss may augment rather than disrupt consumer–prey interactions, and this will depend greatly on the degree of specialization of functionally dominant natural enemies.     

What does engram encode?: Heterogeneous memory engrams for different aspects of experience

Long-lasting synaptic changes within the neuronal network mediate memory. Neurons bearing such physical traces of memory (memory engram cells) are often equated with neurons expressing immediate early genes (IEGs) during a specific experience. However, past studies observed the expression of different IEGs in non-overlapping neurons or synaptic plasticity in neurons that do not express a particular IEG. Importantly, recent studies revealed that distinct subsets of neurons expressing different IEGs or even IEG negative-(yet active) neurons support different aspects of memory or computation, suggesting a more complex nature of memory engram cells than previously thought. In this short review, we introduce studies revealing such heterogeneous composition of the memory engram and discuss how the memory system benefits from it.     

Variation in migration propensity among individuals maintained by landscape structure

Metapopulation dynamics lead to predictable patterns of habitat occupancy, population density and trophic structure in relation to landscape features such as habitat patch size and isolation. Comparable patterns may occur in behavioural, physiological and life‐history traits but remain little studied. In the Glanville fritillary butterfly, females in newly established populations were more mobile than females in old populations. Among females from new populations, mobility decreased with increasing connectivity (decreasing isolation), but in females from old populations mobility increased with connectivity. The [ATP]/[ADP] ratio of flight muscles following controlled activity showed the same pattern as mobility in relation to population age and connectivity, suggesting that physiological differences in flight metabolic performance contribute to the observed variation in mobility. We demonstrate with an evolutionary metapopulation model parameterised for the Glanville fritillary that increasing spatial variation in landscape structure increases variance in mobility among individuals in a metapopulation, supporting the general notion that complex landscape structure maintains life‐history variation.     

The anatomy of predator-prey dynamics in a changing climate

Humans are increasingly influencing global climate and regional predator assemblages, yet a mechanistic understanding of how climate and predation interact to affect fluctuations in prey populations is currently lacking. Here we develop a modelling framework to explore the effects of different predation strategies on the response of age-structured prey populations to a changing climate. We show that predation acts in opposition to temporal correlation in climatic conditions to suppress prey population fluctuations. Ambush predators such as lions are shown to be more effective at suppressing fluctuations in their prey than cursorial predators such as wolves, which chase down prey over long distances, because they are more effective predators on prime-aged adults. We model climate as a Markov process and explore the consequences of future changes in climatic autocorrelation for population dynamics. We show that the presence of healthy predator populations will be particularly important in dampening prey population fluctuations if temporal correlation in climatic conditions increases in the future.     

SPATIALLY CORRELATED EXTINCTIONS SELECT FOR LESS EMIGRATION BUT LARGER DISPERSAL DISTANCES IN THE SPIDER MITE TETRANYCHUS URTICAE

Dispersal is a central process to almost all species on earth, as it connects spatially structured populations and thereby increases population persistence. Dispersal is subject to (rapid) evolution and local patch extinctions are an important selective force in this context. In contrast to the randomly distributed local extinctions considered in most theoretical studies, habitat fragmentation or other anthropogenic interventions will lead to spatially correlated extinction patterns. Under such conditions natural selection is thought to lead to more long‐distance dispersal, but this theoretical prediction has not yet been verified empirically. We test this prediction in experimental spatially structured populations of the spider mite Tetranychus urticae and supplement these empirical results with insights from an individual‐based evolutionary model. We demonstrate that the spatial correlation of local extinctions changes the entire distribution of dispersal distances (dispersal kernel) and selects for overall less emigration but more long‐distance dispersal.     

From survivors to replicators: evolution by natural selection revisited

For evolution by natural selection to occur it is classically admitted that the three ingredients of variation, difference in fitness and heredity are necessary and sufficient. In this paper, I show using simple individual-based models, that evolution by natural selection can occur in populations of entities in which neither heredity nor reproduction are present. Furthermore, I demonstrate by complexifying these models that both reproduction and heredity are predictable Darwinian products (i.e. complex adaptations) of populations initially lacking these two properties but in which new variation is introduced via mutations. Later on, I show that replicators are not necessary for evolution by natural selection, but rather the ultimate product of such processes of adaptation. Finally, I assess the value of these models in three relevant domains for Darwinian evolution.     

Losses of female song with changes from tropical to temperate breeding in the New World blackbirds

Birds in which both sexes produce complex songs are thought to be more common in the tropics than in temperate areas, where typically only males sing. Yet the role of phylogeny in this apparent relationship between female song and latitude has never been examined. Here, we reconstruct evolutionary changes in female song and breeding latitude in the New World blackbirds (Icteridae), a family with both temperate and tropical representatives. We provide strong evidence that members of this group have moved repeatedly from tropical to temperate breeding ranges and, furthermore, that these range shifts were associated with losses of female song more often than expected by chance. This historical perspective suggests that male-biased song production in many temperate species is the result not of sexual selection for complex song in males but of selection against such songs in females. Our results provide new insights into the differences we see today between tropical and temperate songbirds, and suggest that the role of sexual selection in the evolution of bird song might not be as simple as we think.     

Bacterial evolution during human infection: Adapt and live or adapt and die

Microbes are constantly evolving. Laboratory studies of bacterial evolution increase our understanding of evolutionary dynamics, identify adaptive changes, and answer important questions that impact human health. During bacterial infections in humans, however, the evolutionary parameters acting on infecting populations are likely to be much more complex than those that can be tested in the laboratory. Nonetheless, human infections can be thought of as naturally occurring in vivo bacterial evolution experiments, which can teach us about antibiotic resistance, pathogenesis, and transmission. Here, we review recent advances in the study of within-host bacterial evolution during human infection and discuss practical considerations for conducting such studies. We focus on 2 possible outcomes for de novo adaptive mutations, which we have termed “adapt-and-live” and “adapt-and-die.” In the adapt-and-live scenario, a mutation is long lived, enabling its transmission on to other individuals, or the establishment of chronic infection. In the adapt-and-die scenario, a mutation is rapidly extinguished, either because it carries a substantial fitness cost, it arises within tissues that block transmission to new hosts, it is outcompeted by more fit clones, or the infection resolves. Adapt-and-die mutations can provide rich information about selection pressures in vivo, yet they can easily elude detection because they are short lived, may be more difficult to sample, or could be maladaptive in the long term. Understanding how bacteria adapt under each of these scenarios can reveal new insights about the basic biology of pathogenic microbes and could aid in the design of new translational approaches to combat bacterial infections.     

Will all species with temperature‐dependent sex determination respond the same way to climate change? A reply to Kallimanis (2010)

Recently, Kallimanis (2010) published a paper proposing a mechanism by which temperature‐dependent sex determination (TSD) may play a key role at facilitating species with this strategy to track their climatic niches across space under climate change. Kallimanis hypothesized that TSD species currently inhabiting stable climatic conditions show reduced population growth rates at the edges of their distributional ranges; under warming conditions, these populations will experience faster growth rates and thus are able to colonize new suitable sites. These ideas are based on the assumption that populations of TSD species have balanced sex ratios at the core of their geographic ranges and biased proportions at the edges. However, Kallimanis’ model overlooks complex processes that may produce a more broadly and less predictable aftermath of climate change on TSD species, so we discuss some of his postulates and underlying assumptions. Kallimanis’ model is based only on one of three known TSD strategies in reptiles, thus it lacks generality; and it does not consider the phenological, behavioral, and physiological strategies that TSD species exhibit across their geographic ranges to buffer the potential impacts of climatic variation over the whole reproductive process. We conclude that simple models such as the one proposed by Kallimanis are not broadly applicable; hence, forecasts of TSD species’ responses to climate change will need to be more specific to groups with similar ecologies and modes of TSD.     

Extreme genetic structure in a social bird species despite high dispersal capacity

Social barriers have been shown to reduce gene flow and contribute to genetic structure among populations in species with high cognitive capacity and complex societies, such as cetaceans, apes and humans. In birds, high dispersal capacity is thought to prevent population divergence unless major geographical or habitat barriers induce isolation patterns by dispersal, colonization or adaptation limitation. We report that Iberian populations of the red‐billed chough, a social, gregarious corvid with high dispersal capacity, show a striking degree of genetic structure composed of at least 15 distinct genetic units. Monitoring of marked individuals over 30 years revealed that long‐distance movements over hundreds of kilometres are common, yet recruitment into breeding populations is infrequent and highly philopatric. Genetic differentiation is weakly related to geographical distance, and habitat types used are overall qualitatively similar among regions and regularly shared by individuals of different populations, so that genetic structure is unlikely to be due solely to isolation by distance or isolation by adaptation. Moreover, most population nuclei showed relatively high levels of genetic diversity, suggesting a limited role for genetic drift in significantly differentiating populations. We propose that social mechanisms may underlie this unprecedented level of genetic structure in birds through a pattern of isolation by social barriers not yet described, which may have driven this remarkable population divergence in the absence of geographical and environmental barriers.     

Heterogeneity–diversity relationships in sessile organisms: a unified framework

The hypothesis that environmental heterogeneity promotes species richness by increasing opportunities for niche partitioning is a fundamental paradigm in ecology. However, recent studies suggest that heterogeneity–diversity relationships (HDR) are more complex than expected from this niche‐based perspective, and often show a decrease in richness at high levels of heterogeneity. These findings have motivated ecologists to propose new mechanisms that may explain such deviations. Here we provide an overview of currently recognised mechanisms affecting the shape of HDRs and present a conceptual model that integrates all previously proposed mechanisms within a unified framework. We also translate the proposed framework into an explicit community dynamic model and use the model as a tool for generating testable predictions concerning how landscape properties interact with species traits in determining the shape of HDRs. Our main finding is that, despite the enormous complexity of such interactions, the predicted HDRs are rather simple, ranging from positive to unimodal patterns in a highly consistent and predictable manner.     

Visual exploration of alternative taxonomies through concepts

A graphical user interface is presented that allows users of taxonomic data to explore concept relationships between conflicting but related taxonomic classifications.Ecological analyses that use taxonomic metadata depend on accurate naming of specimens and taxa, and if the metadata involves several taxonomies, care has to be taken to match concepts between them. To perform this accurately requires expert-defined concept relationships, which are more complex yet more representative than the simple one-to-one mappings found through simple name matching, and can accommodate nomenclatural changes and differences in classification technique (cf ‘lumpers’ versus ‘splitters’). In the SEEK-Taxon (Scientific Environment for Ecological Knowledge) project we aim to help users of taxonomic datasets untangle and understand these relationships through a prototype visual interface which graphically displays these relationship structures, allowing users to comprehend such information and more accurately name their data.     

Complex patterns of global spread in invasive insects: eco-evolutionary and management consequences

The advent of simple and affordable tools for molecular identification of novel insect invaders and assessment of population diversity has changed the face of invasion biology in recent years. The widespread application of these tools has brought with it an emerging understanding that patterns in biogeography, introduction history and subsequent movement and spread of many invasive alien insects are far more complex than previously thought. We reviewed the literature and found that for a number of invasive insects, there is strong and growing evidence that multiple introductions, complex global movement, and population admixture in the invaded range are commonplace. Additionally, historical paradigms related to species and strain identities and origins of common invaders are in many cases being challenged. This has major consequences for our understanding of basic biology and ecology of invasive insects and impacts quarantine, management and biocontrol programs. In addition, we found that founder effects rarely limit fitness in invasive insects and may benefit populations (by purging harmful alleles or increasing additive genetic variance). Also, while phenotypic plasticity appears important post-establishment, genetic diversity in invasive insects is often higher than expected and increases over time via multiple introductions. Further, connectivity among disjunct regions of global invasive ranges is generally far higher than expected and is often asymmetric, with some populations contributing disproportionately to global spread. We argue that the role of connectivity in driving the ecology and evolution of introduced species with multiple invasive ranges has been historically underestimated and that such species are often best understood in a global context.     

Selective Strolls: Fixation and Extinction in Diploids Are Slower for Weakly Selected Mutations Than for Neutral Ones

In finite populations, an allele disappears or reaches fixation due to two main forces, selection and drift. Selection is generally thought to accelerate the process: a selected mutation will reach fixation faster than a neutral one, and a disadvantageous one will quickly disappear from the population. We show that even in simple diploid populations, this is often not true. Dominance and recessivity unexpectedly slow down the evolutionary process for weakly selected alleles. In particular, slightly advantageous dominant and mildly deleterious recessive mutations reach fixation slightly more slowly than neutral ones (at most 5%). This phenomenon determines genetic signatures opposite to those expected under strong selection, such as increased instead of decreased genetic diversity around the selected site. Furthermore, we characterize a new phenomenon: mildly deleterious recessive alleles, thought to represent a wide fraction of newly arising mutations, on average survive in a population slightly longer than neutral ones, before getting lost. Consequently, these mutations are on average slightly older than neutral ones, in contrast with previous expectations. Furthermore, they slightly increase the amount of weakly deleterious polymorphisms, as a consequence of the longer unconditional sojourn times compared to neutral mutations.     

Auditory cortex: comparative aspects of maps and plasticity.

Much recent work in the field of auditory cortex analysis consists of an intensified search for complex sound representation and sound localization mechanisms using tonotopic maps as a frame of reference. Mammalian species rely on parallel processing in multiple tonotopic and non-tonotopic maps but show different degrees of unit complexity, and orderly representation of acoustic dimensions in such maps depending on the predictability of sounds in their environment. Birds appear to rely chiefly on one tonotopic map which harbours multidimensional complex representations. During development and after partial hearing loss, tonotopic organization changes in a predictable manner. Learning also modifies the spatial representation of sounds and even modifies tonotopic organization, but the spatial rules involved in this process have not yet emerged.     

Foreseeing the future of mutualistic communities beyond collapse

Changing conditions may lead to sudden shifts in the state of ecosystems when critical thresholds are passed. Some well‐studied drivers of such transitions lead to predictable outcomes such as a turbid lake or a degraded landscape. Many ecosystems are, however, complex systems of many interacting species. While detecting upcoming transitions in such systems is challenging, predicting what comes after a critical transition is terra incognita altogether. The problem is that complex ecosystems may shift to many different, alternative states. Whether an impending transition has minor, positive or catastrophic effects is thus unclear. Some systems may, however, behave more predictably than others. The dynamics of mutualistic communities can be expected to be relatively simple, because delayed negative feedbacks leading to oscillatory or other complex dynamics are weak. Here, we address the question of whether this relative simplicity allows us to foresee a community's future state. As a case study, we use a model of a bipartite mutualistic network and show that a network's post‐transition state is indicated by the way in which a system recovers from minor disturbances. Similar results obtained with a unipartite model of facilitation suggest that our results are of relevance to a wide range of mutualistic systems.     

Fish assemblages as indicators of estuary ecosystem health

Understanding and managing increasing threat from diverse anthropogenic pressures on estuaries requires impact assessment and monitoring indices that provide accurate quantification of change and are readily communicable. Although indices based on nekton assemblage structure have obvious appeal to managers, the imperative to produce the most accurate measures possible has seen a move away from simple composite measures (such as diversity indices) towards complex multivariate approaches. However, complex methods often provide a poor basis for reporting because they can be difficult to report in terms that are meaningful to the end user. Effective indices should be simple to construct and communicate, relate directly to definable biological attributes, fall within predictable ranges for unimpacted systems and show demonstrable responses to known impacts. We use published nekton data for 30 natural and two artificial estuaries to develop a set of nekton assemblage-based summary measures that fit these criteria. We evaluated a suite of simple parallel measures based on both catch per unit effort (CPUE) and probability of encounter (PoE). Parallel measures provide complementary information thus a more robust assessments of change. Three measures fell within consistent bounds as long as comparisons were confined to the same time of year to remove the influence of seasonal variability, and were efficient at differentiating degraded from unimpacted estuaries. Because the successful approaches rely on PoE rather than CPUE they have considerable tactical advantages in that they are less destructive, allow for the collection of many more samples per unit time, and treat schooling and non-schooling species equivalently.     

Reassembly of JIP1 Scaffold Complex in JNK MAP Kinase Pathway Using Heterologous Protein Interactions

Formation of signaling protein complexes is crucial for proper signal transduction. Scaffold proteins in MAP kinase pathways are thought to facilitate complex assembly, thereby promoting efficient and specific signaling. To elucidate the assembly mechanism of scaffold complexes in mammals, we attempted to rationally rewire JIP1-dependent JNK MAP kinase pathway via alternative assembly of JIP1 complex. When JIP1-JNK docking interaction in the complex was replaced with heterologous protein interaction domains, such as PDZ domains and JNK-binding domains, a functional scaffold complex was reconstituted, and JNK signaling was rescued. Reassembly of JIP1 complex using heterologous protein interactions was sufficient for restoring of JNK MAP kinase pathway to induce signaling responses, including JNK activation and cell death. These results suggest a simple yet modular mechanism for JIP1 scaffold assembly in mammals.