GPS tracking data of Eurasian oystercatchers (Haematopusostralegus) from the Netherlands and Belgium.

We describe six datasets that contain GPS and accelerometer data of 202 Eurasian oystercatchers (Haematopusostralegus) spanning the period 2008-2021. Birds were equipped with GPS trackers in breeding and wintering areas in the Netherlands and Belgium. We used GPS trackers from the University of Amsterdam Bird Tracking System (UvA-BiTS) for several study purposes, including the study of space use during the breeding season, habitat use and foraging behaviour in the winter season, and impacts of human disturbance. To enable broader usage, all data have now been made open access. Combined, the datasets contain 6.0 million GPS positions, 164 million acceleration measurements and 7.0 million classified behaviour events (i.e., flying, walking, foraging, preening, and inactive). The datasets are deposited on the research repository Zenodo, but are also accessible on Movebank and as down-sampled occurrence datasets on the Global Biodiversity Information Facility (GBIF) and Ocean Biodiversity Information System (OBIS).

An empirical confirmation of diversified bet hedging as a survival strategy in unpredictably varying environments.

Environmental change jeopardizes the survival of species from variable environments by making the occurrence of favorable conditions less predictable. For organisms with long-lived propagules (e.g., spores, eggs, or seeds), the theory of diversified bet hedging (DBH) predicts that delayed hatching over different growing seasons can help populations avoid extinction. Empirical observations in different organisms are consistent with DBH, but integrated tests that simultaneously validate the main theoretical assumptions and predictions are lacking. In this study, we combine field and multi-generational lab experiments to provide a complete test of DBH. Consistent with DBH predictions, resting egg clutches of the fairy shrimp Branchipodopsis wolfi, which inhabits rain-fed temporary rock pool environments with unpredictable inundations, hatched partially over a succession of inundations with identical hatching cues. Bet hedging was more common in populations from more unpredictable habitats where hatching fractions were lower. This differentiation in hatching strategies was preserved after two generations under common garden conditions, which implies intrinsic (epi-)genetic control of hatching. Finally, a demographic model confirmed that lower hatching fractions increase long-term population growth in unpredictable habitats. With this paper we propose a method to calculate probabilities of successful recruitment for organisms that use imperfect cues and show that this drives selection for variation in life history strategies as part of a DBH strategy.

GPS tracking data of Western marsh harriers breeding in Belgium and the Netherlands.

In this data paper three datasets are described containing GPS tracking and acceleration data of Western marsh harriers (Circus aeruginosus) breeding in Belgium and the Netherlands. The Western marsh harrier is included as a threatened bird species in Annex I of the European Bird Directive due to the steep decline in population densities. In order to collect data of habitat use and migration behaviour, Western marsh harriers were equipped with light-weight solar powered GPS trackers developed by the Institute for Biodiversity and Ecosystem Dynamics (IBED) at the University of Amsterdam (University of Amsterdam Bird Tracking System, UvA-BiTS). These trackers automatically collect and store data on the bird's activity and 3D position in time and transmit these data to ground stations. The datasets were collected by the Research Institute for Nature and Forest (INBO) and the Dutch Montagu's Harrier Foundation. Tracked Western marsh harriers were breeding in the northeast of the Dutch province of Groningen and on the opposite side of the river Ems in Germany (H_GRONINGEN), in the region of Waterland-Oudeman near the Belgian-Dutch border (MH_WATERLAND), and at the left bank of the Scheldt estuary, close to the Belgian-Dutch border and north of the city of Antwerp (MH_ANTWERPEN). Most individuals remained within 10 km from their nesting sites during the breeding season and wintered in West Africa. H_GRONINGEN contains 987,493 GPS fixes and 3,853,859 acceleration records of four individuals since 2012. MH_WATERLAND contains 377,910 GPS fixes of seven individuals. Sampling in this region began in 2013. Three more Western marsh harriers were tagged in the Scheldt estuary near Antwerp more recently in 2018 (one individual) and 2019 (two individuals) for the MH_ANTWERPEN study, which contains 47,917 GPS fixes and 227,746 acceleration records. The three Western marsh harrier datasets were published as separate studies in Movebank (https://www.movebank.org) and archived as data packages in Zenodo (https://www.zenodo.org) to ensure long-term preservation and versioning of the data.

Regional neutrality evolves through local adaptive niche evolution.

Biodiversity in natural systems can be maintained either because niche differentiation among competitors facilitates stable coexistence or because equal fitness among neutral species allows for their long-term cooccurrence despite a slow drift toward extinction. Whereas the relative importance of these two ecological mechanisms has been well-studied in the absence of evolution, the role of local adaptive evolution in maintaining biological diversity through these processes is less clear. Here we study the contribution of local adaptive evolution to coexistence in a landscape of interconnected patches subject to disturbance. Under these conditions, early colonists to empty patches may adapt to local conditions sufficiently fast to prevent successful colonization by other preadapted species. Over the long term, the iteration of these local-scale priority effects results in niche convergence of species at the regional scale even though species tend to monopolize local patches. Thus, the dynamics evolve from stable coexistence through niche differentiation to neutral cooccurrence at the landscape level while still maintaining strong local niche segregation. Our results show that neutrality can emerge at the regional scale from local, niche-based adaptive evolution, potentially resolving why ecologists often observe neutral distribution patterns at the landscape level despite strong niche divergence among local communities.

The heat is on: Genetic adaptation to urbanization mediated by thermal tolerance and body size.

Worldwide, urbanization leads to tremendous anthropogenic environmental alterations, causing strong selection pressures on populations of animals and plants. Although a key feature of urban areas is their higher temperature ("urban heat islands"), adaptive thermal evolution in organisms inhabiting urban areas has rarely been studied. We tested for evolution of a higher heat tolerance (CTMAX ) in urban populations of the water flea Daphnia magna, a keystone grazer in freshwater ecosystems, by carrying out a common garden experiment at two temperatures (20°C and 24°C) with genotypes of 13 natural populations ordered along a well-defined urbanization gradient. We also assessed body size and haemoglobin concentration to identify underlying physiological drivers of responses in CTMAX . We found a higher CTMAX in animals isolated from urban compared to rural habitats and in animals reared at higher temperatures. We also observed substantial genetic variation in thermal tolerance within populations. Overall, smaller animals were more heat tolerant. While urban animals mature at smaller size, the effect of urbanization on thermal tolerance is only in part caused by reductions in body size. Although urban Daphnia contained higher concentrations of haemoglobin, this did not contribute to their higher CTMAX . Our results provide evidence of adaptive thermal evolution to urbanization in the water flea Daphnia. In addition, our results show both evolutionary potential and adaptive plasticity in rural as well as urban Daphnia populations, facilitating responses to warming. Given the important ecological role of Daphnia in ponds and lakes, these adaptive responses likely impact food web dynamics, top-down control of algae, water quality, and the socio-economic value of urban ponds.

Evolving Perspectives on Monopolization and Priority Effects.

Biologists are often confronted with high levels of unexplained variation when studying the processes that determine genetic and species diversity. Here, we argue that eco-evolutionary interactions might often play an important role during colonization and have longstanding effects on populations and communities. Adaptation following colonization can produce a strong positive feedback loop that promotes priority effects and context-dependent trajectories of population or species assembly. We establish how monopolization, and more generally evolution-mediated priority effects, influence ecological patterns at multiple scales of space, time, and biological organization. We then highlight the underappreciated implications for our understanding of population and landscape genetics, adaptive evolution, community diversity, biogeography, and conservation biology. We indicate multiple future directions for research, including extending theory beyond competition.

Inbreeding and adaptive plasticity: an experimental analysis on predator-induced responses in the water flea Daphnia.

Several studies have emphasized that inbreeding depression (ID) is enhanced under stressful conditions. Additionally, one might imagine a loss of adaptively plastic responses which may further contribute to a reduction in fitness under environmental stress. Here, we quantified ID in inbred families of the cyclical parthenogen Daphnia magna in the absence and presence of fish predation risk. We test whether predator stress affects the degree of ID and if inbred families have a reduced capacity to respond to predator stress by adaptive phenotypic plasticity. We obtained two inbred families through clonal selfing within clones isolated from a fish pond. After mild purging under standardized conditions, we compared life history traits and adaptive plasticity between inbred and outbred lineages (directly hatched from the natural dormant egg bank of the same pond). Initial purging of lineages under standardized conditions differed among inbred families and exceeded that in outbreds. The least purged inbred family exhibited strong ID for most life history traits. Predator-induced stress hardly affected the severity of ID, but the degree to which the capacity for adaptive phenotypic plasticity was retained varied strongly among the inbred families. The least purged family overall lacked the capacity for adaptive phenotypic plasticity, whereas the family that suffered only mild purging exhibited a potential for adaptive plasticity that was comparable to the outbred population. We thus found that inbred offspring may retain the capacity to respond to the presence of fish by adaptive phenotypic plasticity, but this strongly depends on the parental clone engaging in selfing.

Experimental evolution reveals high insecticide tolerance in Daphnia inhabiting farmland ponds.

Exposure of nontarget populations to agricultural chemicals is an important aspect of global change. We quantified the capacity of natural Daphnia magna populations to locally adapt to insecticide exposure through a selection experiment involving carbaryl exposure and a control. Carbaryl tolerance after selection under carbaryl exposure did not increase significantly compared to the tolerance of the original field populations. However, there was evolution of a decreased tolerance in the control experimental populations compared to the original field populations. The magnitude of this decrease was positively correlated with land use intensity in the neighbourhood of the ponds from which the original populations were sampled. The genetic change in carbaryl tolerance in the control rather than in the carbaryl treatment suggests widespread selection for insecticide tolerance in the field associated with land use intensity and suggests that this evolution comes at a cost. Our data suggest a strong impact of current agricultural land use on nontarget natural Daphnia populations.

Gene pleiotropy constrains gene expression changes in fish adapted to different thermal conditions.

Understanding the factors that shape the evolution of gene expression is a central goal in biology, but the molecular mechanisms behind this remain controversial. A related major goal is ascertaining how such factors may affect the adaptive potential of a species or population. Here we demonstrate that temperature-driven gene expression changes in fish adapted to differing thermal environments are constrained by the level of gene pleiotropy estimated by either the number of protein interactions or gene biological processes. Genes with low pleiotropy levels were the main drivers of both plastic and evolutionary global expression profile changes, while highly pleiotropic genes had limited expression response to temperature treatment. Our study provides critical insights into the molecular mechanisms by which natural populations can adapt to changing environments. In addition to having important implications for climate change adaptation, these results suggest that gene pleiotropy should be considered more carefully when interpreting expression profiling data.

Drivers of population genetic differentiation in the wild: isolation by dispersal limitation, isolation by adaptation and isolation by colonization.

Empirical population genetic studies have been dominated by a neutralist view, according to which gene flow and drift are the main forces driving population genetic structure in nature. The neutralist view in essence describes a process of isolation by dispersal limitation (IBDL) that generally leads to a pattern of isolation by distance (IBD). Recently, however, conceptual frameworks have been put forward that view local genetic adaptation as an important driver of population genetic structure. Isolation by adaptation (IBA) and monopolization (M) posit that gene flow among natural populations is reduced as a consequence of local genetic adaptation. IBA stresses that effective gene flow is reduced among habitats that show dissimilar ecological characteristics, leading to a pattern of isolation by environment. In monopolization, local genetic adaptation of initial colonizing genotypes results in a reduction in gene flow that fosters the persistence of founder effects. Here, we relate these different processes driving landscape genetic structure to patterns of IBD and isolation by environment (IBE). We propose a method to detect whether IBDL, IBA and M shape genetic differentiation in natural landscapes by studying patterns of variation at neutral and non-neutral markers as well as at ecologically relevant traits. Finally, we reinterpret a representative number of studies from the recent literature by associating patterns to processes and identify patterns associated with local genetic adaptation to be as common as IBDL in structuring regional genetic variation of populations in the wild. Our results point to the importance of quantifying environmental gradients and incorporating ecology in the analysis of population genetics.

The role of selection in driving landscape genomic structure of the waterflea Daphnia magna.

The combined analysis of neutral and adaptive genetic variation is crucial to reconstruct the processes driving population genetic structure in the wild. However, such combined analysis is challenging because of the complex interaction among neutral and selective processes in the landscape. Overcoming this level of complexity requires an unbiased search for the evidence of selection in the genomes of populations sampled from their natural habitats and the identification of demographic processes that lead to present-day populations' genetic structure. Ecological model species with a suite of genomic tools and well-understood ecologies are best suited to resolve this complexity and elucidate the role of selective and demographic processes in the landscape genomic structure of natural populations. Here we investigate the water flea Daphnia magna, an emerging model system in genomics and a renowned ecological model system. We infer past and recent demographic processes by contrasting patterns of local and regional neutral genetic diversity at markers with different mutation rates. We assess the role of the environment in driving genetic variation in our study system by identifying correlates between biotic and abiotic variables naturally occurring in the landscape and patterns of neutral and adaptive genetic variation. Our results indicate that selection plays a major role in determining the population genomic structure of D. magna. First, environmental selection directly impacts genetic variation at loci hitchhiking with genes under selection. Second, priority effects enhanced by local genetic adaptation (cf. monopolization) affect neutral genetic variation by reducing gene flow among populations and genetic diversity within populations.

Genotype × genotype interactions between the toxic cyanobacterium Microcystis and its grazer, the waterflea Daphnia.

Toxic algal blooms are an important problem worldwide. The literature on toxic cyanobacteria blooms in inland waters reports widely divergent results on whether zooplankton can control cyanobacteria blooms or cyanobacteria suppress zooplankton by their toxins. Here we test whether this may be due to genotype × genotype interactions, in which interactions between the large-bodied and efficient grazer Daphnia and the widespread cyanobacterium Microcystis are not only dependent on Microcystis strain or Daphnia genotype but are specific to genotype × genotype combinations. We show that genotype × genotype interactions are important in explaining mortality in short-time exposures of Daphnia to Microcystis. These genotype × genotype interactions may result in local coadaptation and a geographic mosaic of coevolution. Genotype × genotype interactions can explain why the literature on zooplankton-cyanobacteria interactions is seemingly inconsistent, and provide hope that zooplankton can contribute to the suppression of cyanobacteria blooms in restoration projects.

A crucial step toward realism: responses to climate change from an evolving metacommunity perspective.

We need to understand joint ecological and evolutionary responses to climate change to predict future threats to biological diversity. The 'evolving metacommunity' framework emphasizes that interactions between ecological and evolutionary mechanisms at both local and regional scales will drive community dynamics during climate change. Theory suggests that ecological and evolutionary dynamics often interact to produce outcomes different from those predicted based on either mechanism alone. We highlight two of these dynamics: (i) species interactions prevent adaptation of nonresident species to new niches and (ii) resident species adapt to changing climates and thereby prevent colonization by nonresident species. The rate of environmental change, level of genetic variation, source-sink structure, and dispersal rates mediate between these potential outcomes. Future models should evaluate multiple species, species interactions other than competition, and multiple traits. Future experiments should manipulate factors such as genetic variation and dispersal to determine their joint effects on responses to climate change. Currently, we know much more about how climates will change across the globe than about how species will respond to these changes despite the profound effects these changes will have on global biological diversity. Integrating evolving metacommunity perspectives into climate change biology should produce more accurate predictions about future changes to species distributions and extinction threats.

Land use, genetic diversity and toxicant tolerance in natural populations of Daphnia magna.

Provided that gene flow is not too high, selection by local environmental conditions in heterogeneous landscapes can lead to genetic adaptation of natural populations to their local habitat. Pollution with anthropogenic toxicants may create pronounced environmental gradients that impose strong local selection pressures. Toxic contaminants may also directly impact genetic structure in natural populations by exhibiting genotoxicity or by causing population declines resulting in genetic bottlenecks. Using populations of Daphnia magna established from the dormant egg banks of ponds located in a landscape dominated by anthropogenic impact, we aimed at detecting evidence for local adaptation to environmental contamination. We explored the relationship between land use around the 10 investigated ponds, population genetic diversity as measured by neutral genetic markers (polymorphic allozymes) and the tolerance of the populations originating from these ponds to acute lethal effects of two model toxicants, the pesticide carbaryl and the metal potassium dichromate. Genetic diversity of the populations as observed by neutral markers tended to be negatively impacted by agricultural land use intensity (Spearman rank correlation, R=-0.614, P=0.059), indicating that genetic bottlenecks may have resulted from anthropogenic impact. We experimentally observed differences in susceptibility to both carbaryl and potassium dichromate among the studied pond populations of D. magna (analysis of deviance, P<0.001). Because the experimental design excluded the possibility of physiological adaptation of the test animals to the toxicants, we conclude that the differences in susceptibility must have a genetic basis. Moreover, carbaryl tolerance levels of the populations tended to increase with increasing agricultural land use intensity as described by ranked percentage of land coverage with cereal and corn crop in the proximity of the ponds (Spearman rank correlation, R=0.602, P=0.066). Together, these two findings provide evidence for local adaptation of D. magna populations to pesticide contamination. Overall, the results demonstrate the potential selection pressure imposed by anthropogenic pollution and provide evidence that genetic erosion in natural Daphnia populations is related to anthropogenic impact.

Extinction, recolonization, and dispersal through time in a planktonic crustacean.

Dormant propagule banks are important reservoirs of biological and genetic diversity of local communities and populations and provide buffering mechanisms against extinction. Although dormant stages of various plant and animal species are known to remain viable for decades and even centuries, little is known about the effective influence of recolonization from such old sources on the genetic continuity of intermittent populations under natural conditions. Using recent and old dormant eggs recovered from a dated lake sediment core in Kenya, we traced the genetic composition of a local population of the planktonic crustacean Daphnia barbata through a sequence of extinction and recolonization events. This was combined with a phylogeographic and population-genetic survey of regional populations. Four successive populations, fully separated in time, inhabited Lake Naivasha from ca. 1330 to 1570 AD, from ca. 1610 to 1720 AD, from ca. 1840 to 1940 AD, and from 1995 to the present (2001 AD). Our results strongly indicate genetic continuity between the 1840-1940 and 1995-2001 populations, which are separated in time by at least 50 years, and close genetic relatedness of them both to the 1330-1580 population. A software tool (Colonize) was developed to find the most likely source population of the refounded 1995-2001 population and to test the number of colonists involved in the recolonization event. The results confirmed that the 1995-2001 population most probably developed out of a limited number of surviving local dormant eggs from the previous population, rather than out of individuals from regional (central and southern Kenya) or more distant (Ethiopia, Zimbabwe) populations that may have immigrated to Lake Naivasha through passive dispersal. These results emphasize the importance of prolonged dormancy for the natural long-term dynamics of crustacean zooplankton in fluctuating environments and suggest an important role of old local dormant egg banks in aquatic habitat restoration.