Priority effects transcend scales and disciplines in biology.

Although primarily studied through the lens of community ecology, phenomena consistent with priority effects appear to be widespread across many different scenarios spanning a broad range of spatial, temporal, and biological scales. However, communication between these research fields is inconsistent and has resulted in a fragmented co-citation landscape, likely due to the diversity of terms used to refer to priority effects across these fields. We review these related terms, and the biological contexts in which they are used, to facilitate greater cross-disciplinary cohesion in research on priority effects. In breaking down these semantic barriers, we aim to provide a framework to better understand the conditions and mechanisms of priority effects, and their consequences across spatial and temporal scales.

Thermal tolerance in the keystone species Daphnia magna-a candidate gene and an outlier analysis approach.

Changes in temperature have occurred throughout Earth's history. However, current warming trends exacerbated by human activities impose severe and rapid loss of biodiversity. Although understanding the mechanisms orchestrating organismal response to climate change is important, remarkably few studies document their role in nature. This is because only few systems enable the combined analysis of genetic and plastic responses to environmental change over long time spans. Here, we characterize genetic and plastic responses to temperature increase in the aquatic keystone grazer Daphnia magna combining a candidate gene and an outlier analysis approach. We capitalize on the short generation time of our species, facilitating experimental evolution, and the production of dormant eggs enabling the analysis of long-term response to environmental change through a resurrection ecology approach. We quantify plasticity in the expression of 35 candidate genes in D. magna populations resurrected from a lake that experienced changes in average temperature over the past century and from experimental populations differing in thermal tolerance isolated from a selection experiment. By measuring expression in multiple genotypes from each of these populations in control and heat treatments, we assess plastic responses to extreme temperature events. By measuring evolutionary changes in gene expression between warm- and cold-adapted populations, we assess evolutionary response to temperature changes. Evolutionary response to temperature increase is also assessed via an outlier analysis using EST-linked microsatellite loci. This study provides the first insights into the role of plasticity and genetic adaptation in orchestrating adaptive responses to environmental change in D. magna.

Improving the forecast for biodiversity under climate change.

New biological models are incorporating the realistic processes underlying biological responses to climate change and other human-caused disturbances. However, these more realistic models require detailed information, which is lacking for most species on Earth. Current monitoring efforts mainly document changes in biodiversity, rather than collecting the mechanistic data needed to predict future changes. We describe and prioritize the biological information needed to inform more realistic projections of species' responses to climate change. We also highlight how trait-based approaches and adaptive modeling can leverage sparse data to make broader predictions. We outline a global effort to collect the data necessary to better understand, anticipate, and reduce the damaging effects of climate change on biodiversity.

Rapid evolution of antioxidant defence in a natural population of Daphnia magna.

Natural populations can cope with rapid changes in stressors by relying on sets of physiological defence mechanisms. Little is known onto what extent these physiological responses reflect plasticity and/or genetic adaptation, evolve in the same direction and result in an increased defence ability. Using resurrection ecology, we studied how a natural Daphnia magna population adjusted its antioxidant defence to ultraviolet radiation (UVR) during a period with increasing incident UVR reaching the water surface. We demonstrate a rapid evolution of the induction patterns of key antioxidant enzymes under UVR exposure in the laboratory. Notably, evolutionary changes strongly differed among enzymes and mainly involved the evolution of UV-induced plasticity. Whereas D. magna evolved a strong plastic up-regulation of glutathione peroxidase under UVR, it evolved a lower plastic up-regulation of glutathione S-transferase and superoxide dismutase and a plastic down-regulation of catalase. The differentially evolved antioxidant strategies were collectively equally effective in dealing with oxidative stress because they resulted in the same high levels of oxidative damage (to lipids, proteins and DNA) and lowered fitness (intrinsic growth rate) under UVR exposure. The lack of better protection against UVR may suggest that the UVR exposure did not increase between both periods. Predator-induced evolution to migrate to lower depths that occurred during the same period may have contributed to the evolved defence strategy. Our results highlight the need for a multiple trait approach when focusing on the evolution of defence mechanisms.

Local and regional founder effects in lake zooplankton persist after thousands of years despite high dispersal potential.

We reconstructed the genetic structure of a planktonic crustacean Daphnia longispina living in high mountain lakes and ponds in the Pyrenees to investigate whether it was shaped by persistent founder effects originating shortly after the last glacial maximum or by ongoing dispersal and effective migration (gene flow). We found that the genetic structure can largely be explained by a single colonization event following gradual deglaciation of the Pyrenees ~10 000-15 000 years ago. Nuclear genetic diversity declined steeply from southeast to northwest, suggestive of serial colonization of available habitats with advancing deglaciation. The spatial genetic structure suggests that founder effects were major determinants of the present-day diversity, both at the catchment level and at the level of individual water bodies, further supporting extremely low effective migration rates. This study reveals a prime example of a founder effect that is both long lasting and maintained at small spatial scales. Our data suggest a process of isolation by colonization as a result of strong priority effects and monopolization. We found evidence for the spread of haplotypes with Pyrenean ancestry across the Palaearctic over distances up to 5500 km, although the local genetic structure after colonization was hardly influenced by contemporary dispersal. Finally, our data also suggest that mitochondrial mutation rates in the studied populations were seven times higher than typically assumed. Overall, we show that founder effects can persist for centuries even at small spatial scales at which the potential for dispersal is high.

Body size and dispersal mode as key traits determining metacommunity structure of aquatic organisms.

Relationships between traits of organisms and the structure of their metacommunities have so far mainly been explored with meta-analyses. We compared metacommunities of a wide variety of aquatic organism groups (12 groups, ranging from bacteria to fish) in the same set of 99 ponds to minimise biases inherent to meta-analyses. In the category of passive dispersers, large-bodied groups showed stronger spatial patterning than small-bodied groups suggesting an increasing impact of dispersal limitation with increasing body size. Metacommunities of organisms with the ability to fly (i.e. insect groups) showed a weaker imprint of dispersal limitation than passive dispersers with similar body size. In contrast, dispersal movements of vertebrate groups (fish and amphibians) seemed to be mainly confined to local connectivity patterns. Our results reveal that body size and dispersal mode are important drivers of metacommunity structure and these traits should therefore be considered when developing a predictive framework for metacommunity dynamics.

Permanent genetic resources added to Molecular Ecology Resources Database 1 October 2010-30 November 2010.

This article documents the addition of 277 microsatellite marker loci to the Molecular Ecology Resources Database. Loci were developed for the following species: Ascochyta rabiei, Cambarellus chapalanus, Chionodraco hamatus, Coptis omeiensis, Cynoscion nebulosus, Daphnia magna, Gerbillus nigeriae, Isurus oxyrinchus, Lates calcarifer, Metacarcinus magister, Oplegnathus fasciatus, Pachycondyla verenae, Phaethon lepturus, Pimelodus grosskopfii, Rotylenchulus reniformis, Scomberomorus niphonius, Sepia esculenta, Terapon jarbua, Teratosphaeria cryptica and Thunnus obesus. These loci were cross-tested on the following species: Austropotamobius italicus, Cambarellus montezumae, Cambarellus puer, Cambarellus shufeldtii, Cambarellus texanus, Chionodraco myersi, Chionodraco rastrospinosus, Coptis chinensis, Coptis chinensis var. brevisepala, Coptis deltoidea, Coptis teeta, Orconectes virilis, Pacifastacus leniusculus, Pimelodus bochii, Procambarus clarkii, Pseudopimelodus bufonius, Rhamdia quelen, Sepia andreana, Sepiella maindroni, Thunnus alalunga, Thunnus albacares, Thunnus maccoyii, Thunnus orientalis, Thunnus thynnus and Thunnus tonggol.

Clonal erosion and genetic drift in cyclical parthenogens--the interplay between neutral and selective processes.

The occurrence of alternating phases of clonal and sexual reproduction may strongly impact the interplay between neutral and selective genetic variation in populations. Using a physiologically structured model of the life history of Daphnia, we investigated to what extent clonal erosion associated with selection during the clonal phase affects the genetic structure as observed by neutral markers. Incorporating conservative levels of quantitative genetic variation at 11 physiological and life history traits induces strong clonal erosion, reducing clonal diversity (CD) near the end of the simulations (1000 days) to a level between 1 and 5, even in habitats with high initial CD (10(8) clones). This strong clonal erosion caused by selection can result in reduced genetic diversity, significant excess of heterozygotes and significant genetic differentiation between populations as observed by neutral markers. Our results indicate that, especially in relatively small habitats, clonal selection may strongly impact the genetic structure and may contribute to the often observed high level of neutral genetic differentiation among natural populations of cyclical parthenogens.

Survival selection on escape performance and its underlying phenotypic traits: a case of many-to-one mapping.

Selection often operates not directly on phenotypic traits but on performance which is important as several traits may contribute to a single performance measure (many-to-one mapping). Although largely ignored in the context of selection, this asks for studies that link all relevant phenotypes with performance and fitness. In an enclosure experiment, we studied links between phenotypic traits, swimming performance and survival in two Enallagma damselflies. Predatory dragonflies imposed survival selection for increased swimming propensity and speed only in E. annexum; probably E. aspersum was buffered by the former species' presence. Accordingly, more circular caudal lamellae, structures involved in generating thrust while swimming, were selected for only in E. annexum. Other phenotypic traits that contributed to swimming speed were apparently not under selection, probably because of many-to-one mapping (functional redundancy). Our results indicate that not only the phenotypic distributions of syntopic prey organisms but also many-to-one mapping should be considered when documenting phenotype-performance-fitness relationships.

Conservation of the introgressed European water frog complex using molecular tools.

In Belgium, the Pelophylax esculentus complex has recently been subjected to multiple introductions of non-native water frogs, increasing the occurrence of hybridisation events. In the present study, we tested the reliability of morphometric and recently developed microsatellite tools to identify introgression and to determine the origin of exotic Belgian water frogs. By analysing 150 individuals of each taxon of the P. esculentus complex and an additional 60 specimens of the introduced P. cf. bedriagae, we show that neither of the currently available tools appears to have sufficient power to reliably distinguish all Belgian water frog species. We therefore aimed at increasing the discriminatory power of a microsatellite identification tool by developing a new marker panel with additional microsatellite loci. By adding only two new microsatellite loci (RlCA5 and RlCA1b20), all taxa of the P. esculentus complex could be distinguished from each other with high confidence. Three more loci (Res3, Res5 and Res17) provided a powerful discrimination of the exotic species.

Development and characterization of eight polymorphic microsatellite markers for Daphnia atkinsoni (Crustacea: Ctenodaphnia).

A microsatellite-enriched genomic library was developed for the water flea Daphnia atkinsoni Baird, 1859, a dominant species of intermittent wetlands in Europe. Eight polymorphic microsatellite markers were successfully optimized. Characterization of 77 individuals from Belgium and Spain showed moderate (in the former) to high (in the latter) levels of polymorphism with two to 11 alleles per locus and an observed heterozygosity ranging from 0 to 0.87. Some of these microsatellite markers were successfully amplified in three other Daphnia species (D. magna n = 4, D. similis n = 6; D. obtusa n = 6).

A cryptic invasion within an invasion and widespread introgression in the European water frog complex: consequences of uncontrolled commercial trade and weak international legislation.

In Western Europe, many pond owners introduce amphibians for ornamental purposes. Although indigenous amphibians are legally protected in most European countries, retailers are circumventing national and international legislation by selling exotic nonprotected sibling species. We investigated to what extent non-native species of the European water frog complex (genus Pelophylax) have become established in Belgium, using morphological, mitochondrial and nuclear genetic markers. A survey of 87 sampling sites showed the presence of non-native water frogs at 47 locations, mostly Marsh frogs (Pelophylax ridibundus). Surprisingly, at least 19% of all these locations also harboured individuals with mitochondrial haplotypes characteristic of Anatolian water frogs (Pelophylax cf. bedriagae). Nuclear genotyping indicated widespread hybridization and introgression between P. ridibundus and P. cf. bedriagae. In addition, water frogs of Turkish origin obtained through a licensed retailer, also contained P. ridibundus and P. cf. bedriagae, with identical haplotypes to the wild Belgian populations. Although P. ridibundus might have invaded Belgium by natural range expansion from neighbouring countries, our results suggest that its invasion was at least partly enhanced by commercial trade, with origins as far as the Middle East. Also the invasion and rapid spread of Anatolian lineages, masked by their high morphological similarity to P. ridibundus, is likely the result of unregulated commercial trade. We expect that Anatolian frogs will further invade the exotic as well as the native range of P. ridibundus and other Pelophylax species elsewhere in Western and Central Europe, with risks of large-scale hybridization and introgression.

Plankton biodiversity along a gradient of productivity and its mediation by macrophytes.

We studied the effect of aquatic vegetation on the process of species sorting and community assembly of three functional groups of plankton organisms (phytoplankton, seston-feeding zooplankton, and substrate-dwelling zooplankton) along a primary productivity gradient. We performed an outdoor cattle tank experiment (n = 60) making an orthogonal combination of a primary productivity gradient (four nutrient addition levels: 0, 10, 100, and 1000 microg P/L; N/P ratio: 16) with a vegetation gradient (no macrophytes, artificial macrophytes, and real Elodea nuttallii). We used artificial plants to evaluate the mere effects of plant physical structure independently from other plant effects, such as competition for nutrients or allelopathy. The tanks were inoculated with species-rich mixtures of phytoplankton and zooplankton. Both productivity and macrophytes affected community structure and diversity of the three functional groups. Taxon richness declined with increasing plankton productivity in each functional group according to a nested subset pattern. We found no evidence for unimodal diversity-productivity relationships. The proportional abundance of Daphnia and of colonial Scenedesmus increased strongly with productivity. GLM analyses suggest that the decline in richness of seston feeders was due to competitive exclusion by Daphnia at high productivity. The decline in richness of phytoplankton was probably caused by high Daphnia grazing. However, partial analyses indicate that these explanations do not entirely explain the patterns. Possibly, environmental deterioration associated with high productivity (e.g., high pH) was also responsible for the observed richness decline. Macrophytes had positive effects on the taxon richness of all three functional plankton groups and interacted with the initial productivity gradient in determining their communities. Macrophytes affected the composition and diversity of the three functional groups both by their physical structure and through other mechanisms. Part of the macrophyte effect may be indirect via a reduction of phytoplankton production. Our results also indirectly suggest that the often reported unimodal relationship between primary productivity and diversity in nature may be partially mediated by the tendency of submerged macrophytes to be most abundant at intermediate productivity levels.

Habitat size and the genetic structure of a cyclical parthenogen, Daphnia magna.

In populations of a cyclical parthenogen, the diversity of clonal lineages, derived from sexually produced eggs, declines during the parthenogenetic phase. Even though Daphnia magna populations from small ponds may harbour millions of individuals, we show that observed clonal and allelic diversity in populations from such small water bodies are lower than in populations from larger water bodies. Populations from small water bodies also show significant fluctuations in allele frequencies among years and a stronger among-population genetic differentiation than populations inhabiting larger water bodies. Persistent founder effects can only explain part of these results. Our data link the population genetic structure of cyclical parthenogens to the size of the habitat and suggest that genetic drift is a more prominent feature of populations inhabiting small water bodies than previously thought.

Coping with predator stress: interclonal differences in induction of heat-shock proteins in the water flea Daphnia magna.

Although predation is a strong selection pressure, little is known about the molecular mechanisms to cope with predator stress. This is crucial to understanding of the mechanisms and constraints involved in the evolution of antipredator traits. We quantified the expression of heat-shock protein 60 (Hsp60), a potential marker for predator stress, in four clones of the water flea Daphnia magna, when exposed to fish kairomones. Expression of Hsp60 induction increased after 6 h and returned to base levels after 24 h of predator stress. This suggests that it is a costly transient mechanism to temporarily cope with novel predator stress, before other defences are induced. We found genetic variation in the fixed levels and in the fish-induced levels of Hsp60, which seemed to be linked to each clone's history of fish predation. Our data suggest that Hsp60 can be considered part of a multiple-trait antipredator defence strategy of Daphnia clones to cope with predator stress.

Phylogeography of Daphnia magna in Europe.

The phylogeographical structure of the water flea Daphnia magna in Europe was analysed using a 609-bp fragment of the cytochrome oxidase subunit I gene. Only moderate overall genetic divergence was detected within Europe. We detected four genetically and, to a large extent, geographically distinct phylogroups within Europe. Our results suggest that these groups recolonized large parts of Europe around 100,000 BP from different refugia. Overall, the pattern suggests a high degree of provincialism with a patchy occurrence of specific lineages, thus confirming the highly subdivided genetic structure usually observed in freshwater zooplankton populations. Although the region around the Mediterranean Sea was only sampled patchily, we obtained strong indications for the occurrence of more divergent genetic lineages in this region. Comparing our European samples to samples from North America and Japan revealed a higher level of differentiation, reflecting limited intercontinental dispersal.

Changes in phototactic behavior of Daphnia magna clone C1 242 in response to copper, cadmium and pentachlorophenol.

In order to develop a sound biotechnique for monitoring water quality that builds on the previous experiments carried out in our laboratory, a specific D. magna clone C1 242 was used to study the effects of pollutants on phototactic behavior. In all experiments, the animals showed a stable and repeatable phototactic index approximated 0.2 in the presence and 0.4 in the absence of fish kairomones, which decreased significantly in response to pollutants. There existed no pollutant x fish kairomone interaction, indicating the changes in phototactic behavior of animals imposed by pollutants were independent of the presence of fish kairomones. The detection limits for changes in phototactic behavior of D. magna clone C1 242 are 0.04 mg/L for copper, 0.02 mg/L for cadmium, and 0.80 mg/L for PCP, respectively, quite lower than LC50 (48 h). The changes in phototactic behavior in presence to pollutants occurred quickly (3 h) compared to the period over whole acute toxicity tests. Therefore, D. magna clone C1 242 could be potentially used to monitor water quality. Moreover, the phototactic behavior did not decrease further in the pollutant mixtures employed in our experiments compared to individual pollutants, except in the Cd-PCP treatment. This fact suggests that the formation of water quality criteria must be based upon pollutant mixture tests.

Geographical and genetic distances among zooplankton populations in a set of interconnected ponds: a plea for using GIS modelling of the effective geographical distance.

In systems of interconnected ponds or lakes, the dispersal of zooplankton may be mediated by the active population component, with rivulets and overflows functioning as dispersal pathways. Using a landscape-based approach, we modelled the effective geographical distance among a set of interconnected ponds (De Maten, Genk, Belgium) in a Geographic Information System (GIS) environment. The first model (the Landscape Model; LM) corrects for the presence of direct connections among ponds and was based on the existing landscape structure (i.e. network of connecting elements among ponds, travelling distance and direction of the current). A second model (the Flow Rate Model; FRM) also incorporated field data on flow rates in the connecting elements as the driving force for the passive dispersal of the active zooplankton population component. Finally, the third model (the Dispersal Rate Model; DRM) incorporated field data on zooplankton dispersal rates. An analysis of the pattern of genetic differentiation among Daphnia ambigua populations inhabiting 10 ponds in the pond complex reveals that the effective geographical distance as modelled by the flow rate and the dispersal rate model provide a better approximation of the true rates of genetic exchange among populations than mere Euclidean geographical distances or the landscape model that takes into account solely the presence of physical connections.

Phototactic behavior of Daphnia and the continuous monitoring of water quality: interference of fish kairomones and food quality.

We carried out a laboratory study to evaluate the sensitivity of phototactic behavior of Daphnia magna to sublethal concentrations of pentachlorophenol (PCP) and copper. More specifically, we determined whether the sensitivity of a D. magna clone to those pollutants is influenced by food quality and the presence of fish kairomones. Test animals were fed either unicellular green algae (Scenedesmus acutus) or fresh baker's yeast (Saccharomyces cerevisiae) and were cultured in the presence or absence of fish kairomones. Four concentrations of PCP (0.4, 0.8, 1.2, and 1.6 mg/L PCP) and one concentration of copper (0.02 mg/L Cu2+) in International Standards Organisation (ISO, Geneva, Switzerland) standard medium were applied in the experiments. Animals were exposed for 3 h to the pollutants prior to the experiments. In the absence of fish kairomones, a strong negative relationship between the phototactic index and nominal sublethal concentrations of PCP was found in animals fed either algae or yeast. The sensitivity of the Daphnia clone to sublethal concentrations of PCP was, however, less clear cut in animals fed yeast than in animals fed algae. The detection limit was 0.4 mg/L PCP with algae as food but was as high as 1.2 mg/L PCP when yeast was used as food. The ability to detect sublethal concentrations of copper and PCP using phototactic behavior was lost when the clones were cultured in the presence of fish kairomones. At a concentration of 0.02 mg/L Cu2+ and in the absence of fish kairomones, the D. magna clone tested became significantly less positively phototactic than in the control treatment regardless of the quality of the food used to culture the test animals. These results suggest that assays using the phototactic behavior of Daphnia to monitor water quality should use genetically stable (clonal) material, positively phototactic, and insensitive to the presence of fish kairomones.