Joint symposium on
Eco-Evolutionary dynamics and
Flanders Annual Meeting of Ecology



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Resilience and evolution: oxymoron or partnership?
DAVID ANGELER

Understanding how species are adapted to, cope with and rebound from disturbances is crucial in times when planet Earth undergoes fast change of social-ecological baselines. Big strides have been made in our understanding of evolution of species and communities to the ever-unfolding change of our environment. However, few attempts have been made to use evolutionary concepts and theories to inform evolution at hierarchically higher levels of biological organization; that is, evolution at the ecosystem level. Ecosystems, which subsume population and community processes, undergo complex dynamics to adapt environmental change. The concept of ecological resilience has taken center stage in academic and practitioners circles for scrutinizing adaptation. A hallmark of ecological resilience is the ability of complex (eco)systems to exist in alternative, often stable equilibria. This definition differs fundamentally from other resilience concepts that are often used in population and community ecology, which focus only on recovery (engineering resilience) after disturbances and which have a single equilibrium focus. A large body of theory and empirical evidence has accumulated about the factors that mediate resilience (e.g., structural and functional attributes of species within and across objectively identified scales of ecosystems). Some of these attributes have been explored as early warning indicators to predict when ecosystem resilience is exhausted and a regime shift becomes imminent. Much of this research is correlative and lacks a mechanistic basis. Evolutionary theory and concepts are deemed important to address current knowledge gaps.

The main aim of this lecture is to seek common ground between eco-evolutionary research and resilience theory and strives for identifying points of interaction where both disciplines can cross-pollinate each other. The lecture will give an overview of ecological resilience theory and its quantifiable components. The quantifiable components of resilience might provide the starting points for seeking synergies between eco-evolution and resilience as a systemic feature.
Eco-evolutionary dynamics and patterns of parallel evolution of host and virus populations
LUTZ BECKS

Different lineages of the same species that independently evolve similar adaptations in identical environments (parallel evolution) denote a certain level of repeatability of evolution. Parallel evolution is most frequently found on the phenotypic level, but is less frequently observed looking at the underlying genetic level. Both evolutionary and ecological dynamics, and their feedbacks will affect the evolutionary trajectories at the individuals’ phenotype and genotype, e.g. through changes in population size and bottlenecks, as well as selective sweeps. Using experimental evolution with replicate populations provides a powerful way to replay evolution and test for parallelism of evolution on the phenotypic and genotypic level. Here, we show high levels of phenotypic parallelism (host resistance) between replicate experimental coevolving populations of an asexual eukaryotic host (alga) and a large dsDNA virus. Yet, when examining variants at the genotypic level (point mutations and small indels) we did not find such parallelism in the host populations across replicates. However, all host populations evolved by duplication of a large genomic region, reflecting the parallelism found at the phenotypic level (host resistance). We explain this pattern by rapid changes in demographic and selective sweeps, which can be an inherent part of eco-evolutionary dynamics.
Adaptation from standing genetic variation – the future of marine animals in a rapidly changing world?
PIERRE DE WIT

In this presentation, I will briefly discuss the theoretical importance of standing genetic variation (presumably “neutral” variants present in a population which could become adaptive in a changing environment), and how it might be critical to organisms facing global environmental changes. I will then discuss the peculiarities of the marine system and why adaptation from standing genetic variation could be particularly important here. Finally, I will give some examples from my recent research on gastropods and crustaceans, where I show that standing genetic variation has had an important role in allowing populations to persist in face of changing water carbonate chemistry, salinity and toxic algal blooms.
Host-parasite coevolution in variable temperature environments
ALISON DUNCAN

I will talk about a study investigating coevolution between bacteria and phage (Pseudomonas flourescens and the lytic phage SBWΦ2) under variable temperature environments. In this study we show that the frequency of environmental change between temperatures, permissive (28°C) and stressful (32°C) for the phage, matters for the induction of temporary coevolutionary coldspots. For this study we devised a coevolution score, which enabled us to show how the precise effects of our different temperature environments impacts coevolution through time. We demonstrated that coevolution is arrested only after spending a threshold amount of time, 4 days, at 32°C, thus creating transient, infection-free, refuges for the host. Nevertheless, coevolution resumed immediately upon return to 28°C, and overall linear increases in bacterial resistance, characteristic of arms-race-dynamic coevolution, were observed under all fluctuation regimes. The coevolution score also allowed us to disentangle the effects of host and parasite demography on coevolution. Temperature variation affected population density, providing evidence that eco-evolutionary feedbacks acted through variable bacteria-phage encounter rates. This permits more precise estimates of eco-evolutionary feedbacks occurring in our populations and the mechanisms inducing the emergent phenomena of coevolutionary hot and cold spots.
The eco-evolutionary dynamics of range expansions
EMANUEL FRONHOFER

Understanding and predicting the (macro)ecological and evolutionary dynamics of range expansions and biological invasions is of great ecological and economical interest. While theoretical and comparative work has advanced significantly over the last years, some of the most basic predictions concerning evolutionary changes during range expansions and their feedbacks on ecological dynamics and patterns remain to be tested experimentally. Central predictions that have yet to be tested include that range expansions select for increased dispersiveness at range margins and that population density decreases from range core to range margin due to trade-offs between dispersal and competitive ability. Furthermore, the impacts of environmental gradients and species interactions on the eco-evolutionary dynamics of species ranges remain untested, to name but a few examples.

In order to provide causal evidence in favour or against these predictions we combined theory with range expansion experiments using microcosm landscapes and protists as model organisms. While we find that range expansions indeed select for increased dispersal at range margins we do not find that population densities decrease from range cores to ranges margins. We also find that invasion dynamics are disturbingly insensitive to gradients in local mortality. Biotic interactions differentially impact both ecological and evolutionary dynamics.
Reconstructing the evolutionary history underlying the genomic landscape of species divergence using haplotype-resolved genomes
PIERRE-ALEXANDRE GAGNAIRE

Understanding how genetic variants are arranged into chromosomal haplotypes within individual genomes represents an important source of information for reconstructing the history of species divergence. In particular, haplotype data are useful for detecting signals of historical admixture between divergent lineages, thus allowing a more precise assessment of genome-wide variation in the intensity and the timing of gene flow. Here, we use haplotype-resolved whole-genome sequences to investigate genome-wide differentiation patterns between naturally hybridizing Atlantic and Mediterranean sea bass lineages (Dicentrarchus labrax). We show that genomic islands of increased differentiation tend to map disproportionately to low-recombining regions. In order to reconstruct the sequence of events associated with the formation of genomic islands, we infer sea bass divergence history from the spectrum of shared haplotype lengths. Our results support that divergence has been shaped by several cycles of allopatric isolation and secondary contact between Atlantic and Mediterranean populations during the Pleistocene. The direct identification of introgressed migrant tracts shows that asymmetrical introgression during secondary contact episodes has resulted in a highly heterogeneous distribution of haplotypes of Atlantic origin within Mediterranean genomes. Finally, reconstructing the ancestral diversity of Mediterranean genomes shows that linked selection has also increased the rate of lineage sorting in low-recombining regions during allopatric episodes. Altogether, these results support that the formation of genomic islands in sea bass results from repeated phases of linked selection and reduced introgression in low-recombining regions.
Adaptation or acclimation to urban anthropogenic stressors: A case study of the great tit
CAROLINE ISAKSSON

To estimate the past and future impact of urbanisation on birds, it is important to understand the mechanistic underpinnings of a physiological response to anthropogenic stress. It is well known that air pollution such as nitrogen oxides and particulate matter, directly associated with urban habitats, increases oxidative stress - a state when the detoxifying antioxidant system is overwhelmed by reactive oxidants, which may cause tissue damage linked to disease and pre-mature senescence. Urban great tits (Parus major) have, repeatedly, shown to have a higher antioxidant activity than rural conspecifics, sometimes sufficient enough to prevent tissue damage and sometimes not. Regardless, an increased antioxidant defence is probably not cost free for the urban birds, which is why we need to understand the mechanistic cause(s) for generating this habitat difference in physiology. Is it a result of: i) the evolutionary history (i.e. a strong selection pressure for greater antioxidant capacities in urban habitats); ii) the present environment (i.e. direct physiological up-regulation in response to current urban stressors); or iii) the individual history combined with the present environment (i.e. developmental programming of gene regulation and the potential for match/mis-match between environment and optimal physiological response). By using the European great tit as our model system, we address these three mechanistic pathways for generating variation in antioxidant capacities between populations and individuals.
How is diversity maintained in pathogen populations?
ANNA-LIISA LAINE

Understanding what maintains diversity in host and pathogen populations is the key to predicting short-term risks of infection and risks of pathogen evolution. Natural host and pathogen populations have been shown to support considerable diversity yet the mechanisms maintaining this diversity are unclear. Generally trade-offs in life-history traits has been proposed to the maintenance of diversity in natural populations. The fungal pathogen, Podosphaera plantaginis, occurs as a highly dynamic metapopulation with considerable genetic diversity that is unevenly distributed. We find a strong link between ecological and evolutionary dynamics as metapopulation dynamics are the key to understanding both numerical and genetic dynamics of this pathogen. Moreover, we find that strains that represent the most common multi-locus genotypes in the natural pathogen metapopulation exhibit contrasting life-history strategies, suggesting that there are different, but equally successful, ways to persist across space and time. These different life-history strategies are likely to promote the maintenance of variation in wild pathogen populations that are subject to spatial and temporal variation in their environments.
Rapid evolution of dispersal modifies the ecological dynamics of biological invasion
TOM MILLER

Ecologists are increasingly aware that genetic and evolutionary mechanisms can have important effects on the ecological dynamics of biological invasions. Yet, because most invasions in nature are unreplicated and play outover heterogeneous landscapes, quantifying the contributions of these mechanisms can be difficult. I will discuss experimental studies of the eco-evolutionary dynamics of invasive range expansion, using insect populations that spread through replicated mesocosms. First, I will address the role of multiple introductions. Because multiple introductions affect the genetic diversity of incipient invasions, they may influence the dynamics of spread through both short-term (heterosis) and long-term (evolutionary) effects. Our work shows that multiple introductions can accelerate spread, likely through a short-term fitness advantage of outcrossing. Second, I will address the ecological consequences of spatial allele sorting that occurs when variation in dispersal ability has a genetic basis, as it often does. Our experiments show that spatial allele sorting leads to the evolution of increased dispersal ability at expanding invasion fronts, and this increases both the mean invasion speed and its variance. Collectively, this work identifies the ecological importance of genetic and evolutionary processes that are intrinsic features of biological invasions, and highlights the value of studying spread dynamics in simple, controlled, and replicated settings.
A conceptual and empirical framework for unifying trait ecology and community phylogenetics
PEDRO PERES-NETO

Understanding the mechanisms by which species assemble into local communities has a long history in ecology, yet it is one of the most active fields of ecological research today. The study of mechanisms underlying complex spatial patterns of biodiversity has a long and challenging history because of the idea that ecological communities have intractable multidimensional spatial patterns that are hard to describe and explain. Two emerging fields, metacommunity ecology, and trait-based and phylogenetic community ecology have been providing important insights into the complex nature of regional and local processes structuring biodiversity patterns at different spatial scales, though rather independently. Because metacommunity studies are often based on patterns of species distributions and co-occurrence, they tell us little about how community assembly actually results from the interactions between local and regional processes, e.g., Does low connectivity in warmer patches versus high connectivity in colder patches facilitate or hinder species co-existence? Alternatively, trait and phylogenetic community ecology explore how species that share similar traits (morphology, behaviour, physiology) and evolutionary histories (phylogenetic relationships) coexist, though they do not sufficiently examine trait and phylogenetic patterns in relation to local and regional mechanisms, particularly ignoring spatial and multi-scale environmental effects. In this presentation, I will try to summarize the different approaches in trait and community phylogenetics into a single framework compatible with metacommunity ecology that explores local and regional processes underlying species distributions and their patterns of co-occurrence.
Intraspecific variation, environmental heterogeneity, and their influence on metapopulation dynamics in the freshwater snails of Guadeloupe
VIKTOR NILSSON-ÖRTMAN

Many organisms can respond beneficially to prolonged temperature exposures, a phenomenon known as acclimation. Although it is widely believed that acclimation should be beneficial in seasonal environments, it remains poorly understood how latitudinal differences in acclimation will affect biotic interactions under climate change. We present a conceptual model showing how both the magnitude and the rate of seasonal changes in temperature determine the adaptive benefit of acclimation at different latitudes. To test predictions from the model, we performed a microcosm experiment using competing species of damselflies that differ in latitudinal distribution. We find that weakly acclimating high-latitude species can become outcompeted by strongly acclimating mid-latitude species under the seasonality imposed by climate change. These findings highlight the need to incorporate the rate of acclimation in predictive climate change frameworks.
Intraspecific variation, environmental heterogeneity, and their influence on metapopulation dynamics in the freshwater snails of Guadeloupe
JELENA PANTEL

Metapopulation models are often used to understand whether a single species can persist in a landscape with multiple patches of potentially connected habitat. However, these models do not take into account the coexistence of multiple species inhabiting the same landscape. It is currently unclear whether the assembly of metacommunities can be understood by modeling the metapopulation dynamics of multiple species independently of one another or whether a community context, where species influence one another’s extinction and colonization, is needed.

We analyzed metapopulation dynamics for 27 species of freshwater snails inhabiting 278 sites on the island of Guadeloupe, sampled annually from 2001 to 2015. For each species, we used occurrence data to estimate colonization and extinction rates as well as the effects of environmental covariates, such as habitat connectivity and rainfall, using a multistate occupancy model. The Bayesian model estimates the probability of transitioning between occupied and unoccupied states and considers the influence of imperfect species detection and persistence of aestivating snails in dry sites.

For most species in the system, average extinction rates exceeded average colonization rates, but the influence of environmental covariates led to prolonged persistence in some species compared to models where no environmental covariates were considered. Remarkably, the colonization and extinction parameters, inferred only from annual transitions between occupied and unoccupied states of sites and therefore in the absence of any species-specific trait or composition information, represented known dimensions of niche partitioning among the various species. We also successfully modeled intraspecific variation in metapopulation dynamics for one of the species. However, the models do not yet take into account species interactions, and do not consider that the extinction and colonization rates of some species may differ after the extinction of other species. An important next step for metapopulation models is to determine the influence not only of environmental heterogeneity among sites, but also intra- and interspecific biodiversity in the system.
Coping with life in soil: comparative analysis of springtail genomes
DICK ROELOFS

Collembola (springtails) represent a soil-living lineage of hexapods in between insects and crustaceans. Consequently, their genomes may hold key information on the early processes leading to evolution of Hexapoda on land. Recently, we generated transcriptomes and very high quality reference genomes for two collembolan species, Folsomia candida and Orchesella cincta, using Illumina and Pacific Bioscience sequencing platforms.

Total size of O. cincta’s genome is 280 Mbp, while Folsomia’s genome is about 60 Mbp smaller in size. In contrast, F. candida contains 28.734 genes, while O. cincta contains about 20.459 genes. Analysis of synonymous mutation rates among orthologous gene pairs shows that the extended gene repertoire in Folsomia was caused by whole genome duplication. Also, extensive gene family expansions and contractions seem to have driven the divergence between the two springtail species. Several expanded gene families could be linked to evolution of stress tolerance in the soil. Still, about 30% of gene clusters did not show any homology to organisms in genome databases, suggesting that they evolved de novo in springtails.

About 1.5-1.8% of the genes have evolved after horizontal gene transfer (HGT) events. Remarkably, a gene cluster resembling a complete functional antibiotic biosynthesis pathway could be identified among HGT genes in Folsomia, and active ß-lactam compounds could be detected in vivo. This is in line with previous observations that Folsomia is very resistant to microbial pathogens, which are abundant among soil microbial communities. Finally, an unusual high number of HGT genes in both springtail genomes seem to originate from fungi. They mostly code for enzymes involved in cell wall degradation, suggesting that they were instrumental in adaptation to specific food resources in the soil ecosystem. I will discuss these findings in the context of arthropod evolution.
Eco-evolutionary resilience in the Anthropocene
MARC URBAN

Understanding the resilience of natural systems to anthropogenic disturbances is necessary to predict and ameliorate future impacts on biodiversity and ecosystem dynamics. Yet, most research fails to address one or more of these fundamental forms of resilience, and these gaps currently limit our ability to predict ecological responses with accuracy. Here I evaluate evidence for both ecological and evolutionary resilience in response to the climate-fueled expansion of an apex predator in temporary ponds. Results demonstrate that the apex predator is substantially affecting community and ecosystem properties in whole-pond manipulations. Experiments show that two prey species have adapted to the predator at fine scales at one field site. We show how these adaptations could increase the resilience of some, but not all, ecological properties of ponds. However, populations located outside of the current marbled salamander range are adapted to other selection regimes that could interfere with these dynamics as the predator spreads north. Understanding the full complexity of both ecological and evolutionary responses will often be necessary to predict the future of biodiversity and ecosystems in the Anthropocene.




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