A millennial‐scale chronicle of evolutionary responses to cultural eutrophication in Daphnia

For an accurate assessment of the anthropogenic impacts on evolutionary change in natural populations, we need long‐term environmental, genetic and phenotypic data that predate human disturbances. Analysis of c. 1600 years of history chronicled in the sediments of South Center Lake, Minnesota, USA, revealed major environmental changes beginning c. 120 years ago coinciding with the initiation of industrialised agriculture in the catchment area. Population genetic structure, analysed using DNA from dormant eggs of the keystone aquatic herbivore, Daphnia pulicaria, suggested no change for c. 1500 years prior to striking shifts associated with anthropogenic environmental alterations. Furthermore, phenotypic assays on the oldest resurrected metazoan genotypes (potentially as old as c. 700 years) indicate significant shifts in phosphorus utilisation rates compared to younger genotypes. Younger genotypes show steeper reaction norms with high growth under high phosphorus (P), and low growth under low P, while ‘ancient’ genotypes show flat reaction norms, yet higher growth efficiency under low P. Using this resurrection ecology approach, environmental, genetic and phenotypic data spanning pre‐ and post‐industrialised agricultural eras clearly reveal the evolutionary consequences of anthropogenic environmental change.     

Extended lifespan traded for diapause in Daphnia

1. Most freshwater crustaceans of the genus Daphnia are cyclically parthenogenetic organisms that are well adapted to unstable habitats due to their short life cycle, wide phenotypic plasticity, and the ability to produce protective diapausing eggs in anticipation of environmental deterioration. Short lifespan and heterogonic reproduction are typical features of Daphnia in a broad spectrum of freshwater habitats, from small temporary pools to large permanent lakes. However, in some locations, departures may be observed from this typical life history pattern to obligate asexuality or extended lifespan. 2. A 3‐year field study in a deep ultraoligotrophic fish‐free alpine‐type lake (Czarny Staw in the Tatra mountains in southern Poland) revealed the coexistence of two closely related asexual lineages of Daphnia of the pulex complex, which differ in body colour (transparent versus orange) and in their strategies for surviving long winters. 3. The ‘transparent’ clone of European origin exhibits an ephemeral lifestyle. It completes its life cycle within a single season, forming two generations of active specimens during the short summer and producing diapausing eggs late in the season. Transparent individuals live no longer than 5–6 months in this cold lake and survive winter exclusively in the form of diapausing eggs. 4. Individuals of the ‘orange’ lineage, which are closely related to eastern Nearctic Daphnia pulicaria, exhibit a biennial lifestyle unique to this genus. They do not form diapausing eggs or produce them only occasionally. Instead, they are active throughout the year and live for up to 13–14 months. Reproduction is postponed until the second year of life when food conditions have improved. Rich lipid reserves accumulated in the first season fuel them during the long winter and permit early reproduction the following spring. 5. Possible reasons for the evolution of obligatory parthenogenesis and long lifespan in Daphnia are discussed.     

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 (CT_MAX) 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 CT_MAX. We found a higher CT_MAX 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 CT_MAX. 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.     

Molecular genetic analysis of Daphnia in the English Lake District: species identity, hybridisation and resting egg banks

• 1 Taxonomic issues in many Daphnia species complexes are often confused by a high degree of phenotypic plasticity and by interspecific hybridisation. Here, we employ molecular genetic tools to confirm the species composition and incidence of hybridisation in extant and resting egg populations of Daphnia from Windermere and Esthwaite Water in the English Lake District.
• 2 A combination of species‐diagnostic allozymes and mtDNA, confirms that contemporary populations are dominated by a single species, D. galeata.
• 3 We present the first account of genetic characterisation of dated ‘resting’ eggs using microsatellites and mtDNA, employing PCR‐based DNA recovery, thus providing a temporal dimension to taxonomic patterns. Thirty years ago, two species were present in Esthwaite, D. galeata and D. hyalina, but Windermere populations were dominated by D. galeata only.
• 4 The use of PCR‐based mtDNA RFLP analysis as a species‐diagnostic tool, and microsatellites to monitor clonal diversity, provide a valuable approach for long‐term studies, especially in populations free from the complicating effect of frequent hybridisation. The detailed limnological records available for many large lakes, and associated changes in land‐use, pollutants and climate, combined with long‐term ephippial molecular genetic data, provide opportunities for exploring natural and anthropogenic impacts on genetic and community structure.

     

Genomic dissection of pod shattering in common bean: mutations at non‐orthologous loci at the basis of convergent phenotypic evolution under domestication of leguminous species

The complete or partial loss of shattering ability occurred independently during the domestication of several crops. Therefore, the study of this trait can provide an understanding of the link between phenotypic and molecular convergent evolution. The genetic dissection of ‘pod shattering’ in Phaseolus vulgaris is achieved here using a population of introgression lines and next‐generation sequencing techniques. The ‘occurrence’ of the indehiscent phenotype (indehiscent versus dehiscent) depends on a major locus on chromosome 5. Furthermore, at least two additional genes are associated with the ‘level’ of shattering (number of shattering pods per plant: low versus high) and the ‘mode’ of shattering (non‐twisting versus twisting pods), with all of these loci contributing to the phenotype by epistatic interactions. Comparative mapping indicates that the major gene identified on common bean chromosome 5 corresponds to one of the four quantitative trait loci for pod shattering in Vigna unguiculata. None of the loci identified comprised genes that are homologs of the known shattering genes in Glycine max. Therefore, although convergent domestication can be determined by mutations at orthologous loci, this was only partially true for P. vulgaris and V. unguiculata, which are two phylogenetically closely related crop species, and this was not the case for the more distant P. vulgaris and G. max. Conversely, comparative mapping suggests that the convergent evolution of the indehiscent phenotype arose through mutations in different genes from the same underlying gene networks that are involved in secondary cell‐wall biosynthesis and lignin deposition patterning at the pod level.     

Multiple simultaneous treatments change plant response from adaptive parental effects to within‐generation plasticity,in Arabidopsis thaliana

In general, studies on plant phenotypic plasticity concentrate on plant responses to different levels of a single environmental factor. Under natural conditions, however, multiple environmental factors often vary simultaneously. I studied the consequences for lifetime fitness caused by single treatments or treatment combinations by investigating patterns of phenotypic plasticity within and between generations. The parental plants (three genotypes of the annual plant Arabidopsis thaliana) received zero, one or two stress treatments at an early life‐stage. The treatments included wounding, shading, chilling, and their pairwise combinations. In the second generation, offspring of treated plants received either the parental or no treatment. Offspring of non‐treated plants were reared under all treatment conditions. Plants responded strongly to the treatments, especially through delayed reproduction, which positively affected lifetime fitness. Notably, treatment combinations triggered stronger plastic responses on average. Because the delay in reproduction was offset by a delay in senescence, the treatments resulted in a fitness gain instead of a loss. However, under adverse environmental conditions, this delay represents a potential fitness cost, especially when the time for reproduction is limited. The treatments ‘wounding’ and ‘shading’ triggered parental effects that increased fitness only in plants that themselves received the treatment. Untreated offspring of wounded or shaded parents performed like control plants. Also, these parental effects were not accompanied by potential fitness costs, such as delayed reproduction. Chilling triggered genotype‐specific parental effects that increased or reduced fitness. Of the treatment combinations only ‘wounding’ and ‘shading’ resulted in genotype‐specific parental effects that increased or reduced fitness independently of offspring treatment. These results suggest that the response of annual plants to treatment combinations triggers predominantly within‐generation plastic responses that include potential fitness costs, which cannot be inferred from studies that manipulate environmental factors individually. Therefore, single treatment studies likely underestimate the costs of plasticity in natural environments.     

Paleogenetic records of Daphnia pulicaria in two North American lakes reveal the impact of cultural eutrophication

Understanding the evolutionary consequences of the green revolution, particularly in wild populations, is an important frontier in contemporary biology. Because human impacts have occurred at varying magnitudes or time periods depending on the study ecosystem, evolutionary histories may vary considerably among populations. Paleogenetics in conjunction with paleolimnology enable us to associate microevolutionary dynamics with detailed information on environmental change. We used this approach to reconstruct changes in the temporal population genetic structure of the keystone zooplankton grazer, Daphnia pulicaria, using dormant eggs extracted from sediments in two Minnesota lakes (South Center, Hill). The extent of agriculture and human population density in the catchment of these lakes has differed markedly since European settlement in the late 19th century and is reflected in their environmental histories reconstructed here. The reconstructed environments of these two lakes differed strongly in terms of environmental stability and their associated patterns of Daphnia population structure. We detected long periods of stability in population structure and environmental conditions in South Center Lake that were followed by a dramatic temporal shift in population genetic structure after the onset of European settlement and industrialized agriculture in its watershed. In particular, we noted a 24.3‐fold increase in phosphorus (P) flux between pre‐European and modern sediment P accumulation rates (AR) in this lake. In contrast, no such shifts were detected in Hill Lake, where the watershed was not as impacted by European settlement and rates of change were less directional with a much smaller increase in sediment P AR (2.3‐fold). We identify direct and indirect effects of eutrophication proxies on genetic structure in these lake populations and demonstrate the power of using this approach in understanding the consequences of anthropogenic environmental change on natural populations throughout historic time periods.     

Complex genotype interactions influence social fitness during the developmental phase of the social amoeba Dictyostelium discoideum

When individuals interact, phenotypic variation can be partitioned into direct genetic effects (DGEs) of the individuals’ own genotypes, indirect genetic effects (IGEs) of their social partners’ genotypes and epistatic interactions between the genotypes of interacting individuals (‘genotype‐by‐genotype (G×G) epistasis’). These components can all play important roles in evolutionary processes, but few empirical studies have examined their importance. The social amoeba Dictyostelium discoideum provides an ideal system to measure these effects during social interactions and development. When starved, free‐living amoebae aggregate and differentiate into a multicellular fruiting body with a dead stalk that holds aloft viable spores. By measuring interactions among a set of natural strains, we quantify DGEs, IGEs and G×G epistasis affecting spore formation. We find that DGEs explain most of the phenotypic variance (57.6%) whereas IGEs explain a smaller (13.3%) but highly significant component. Interestingly, G×G epistasis explains nearly a quarter of the variance (23.0%), highlighting the complex nature of genotype interactions. These results demonstrate the large impact that social interactions can have on development and suggest that social effects should play an important role in developmental evolution in this system.     

Contrasting gene expression programs correspond with predator‐induced phenotypic plasticity within and across generations in Daphnia

Research has shown that a change in environmental conditions can alter the expression of traits during development (i.e., “within‐generation phenotypic plasticity”) as well as induce heritable phenotypic responses that persist for multiple generations (i.e., “transgenerational plasticity”, TGP). It has long been assumed that shifts in gene expression are tightly linked to observed trait responses at the phenotypic level. Yet, the manner in which organisms couple within‐ and TGP at the molecular level is unclear. Here we tested the influence of fish predator chemical cues on patterns of gene expression within‐ and across generations using a clone of Daphnia ambigua that is known to exhibit strong TGP but weak within‐generation plasticity. Daphnia were reared in the presence of predator cues in generation 1, and shifts in gene expression were tracked across two additional asexual experimental generations that lacked exposure to predator cues. Initial exposure to predator cues in generation 1 was linked to ~50 responsive genes, but such shifts were 3–4× larger in later generations. Differentially expressed genes included those involved in reproduction, exoskeleton structure and digestion; major shifts in expression of genes encoding ribosomal proteins were also identified. Furthermore, shifts within the first‐generation and transgenerational shifts in gene expression were largely distinct in terms of the genes that were differentially expressed. Such results argue that the gene expression programmes involved in within‐ vs. transgeneration plasticity are fundamentally different. Our study provides new key insights into the plasticity of gene expression and how it relates to phenotypic plasticity in nature.     

Eutrophication mediates rapid clonal evolution in Daphnia pulicaria

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Phenotypic plasticity of desiccation resistance in Glossina puparia: are there ecotype constraints on acclimation responses?

Phenotypic plasticity allows organisms to cope with environmental variation and may aid in the evolution of novel traits. However, whether phenotypic plasticity is beneficial, or if acclimation responses might be constrained to particular ecotypes is generally poorly explored. Here we test the beneficial acclimation hypothesis (BAH) and its alternatives for desiccation resistance to atmospheric moisture in mesic‐ and xeric‐adapted Glossina species. Highly significant interactions among acclimation and test humidity were detected for water loss rates indicative of significant phenotypic plasticity. Ordered‐factor anova was unable to reject predictions of the ‘drier is better’ acclimation hypothesis in xeric Glossina morsitans and mesic G. austeni. Evidence for the ‘deleterious acclimation hypothesis’ was found for mesic G. palpalis as expected from the moist habitats it typically occupies. By contrast, support for the ‘optimal acclimation hypothesis’ was found in xeric G. pallidipes. Little support for BAH was obtained in the present study, although other hypotheses, which might enhance fitness within the environments these species are typically exposed to, were supported. However, acclimation responses were not necessarily constrained to xeric/mesic ecotypes which might be expected if adaptation to a particular environment arose as a trade‐off between plastic responses and living in a particular habitat. These results highlight the complexity of acclimation responses and suggest an important role for phenotypic plasticity in moderating environmental effects on evolutionary fitness in Glossina.     

Mating patterns influence vulnerability to the extinction vortex

Earth's biodiversity is undergoing mass extinction due to anthropogenic compounding of environmental, demographic and genetic stresses. These different stresses can trap populations within a reinforcing feedback loop known as the extinction vortex, in which synergistic pressures build upon one another through time, driving down population viability. Sexual selection, the widespread evolutionary force arising from competition, choice and reproductive variance within animal mating patterns could have vital consequences for population viability and the extinction vortex: (a) if sexual selection reinforces natural selection to fix ‘good genes’ and purge ‘bad genes’, then mating patterns encouraging competition and choice may help protect populations from extinction; (b) by contrast, if mating patterns create load through evolutionary or ecological conflict, then population viability could be further reduced by sexual selection. We test between these opposing theories using replicate populations of the model insect Tribolium castaneum exposed to over 10 years of experimental evolution under monogamous versus polyandrous mating patterns. After a 95‐generation history of divergence in sexual selection, we compared fitness and extinction of monogamous versus polyandrous populations through an experimental extinction vortex comprising 15 generations of cycling environmental and genetic stresses. Results showed that lineages from monogamous evolutionary backgrounds, with limited opportunities for sexual selection, showed rapid declines in fitness and complete extinction through the vortex. By contrast, fitness of populations from the history of polyandry, with stronger opportunities for sexual selection, declined slowly, with 60% of populations surviving by the study end. The three vortex stresses of (a) nutritional deprivation, (b) thermal stress and (c) genetic bottlenecking had similar impacts on fitness declines and extinction risk, with an overall sigmoid decline in survival through time. We therefore reveal sexual selection as an important force behind lineages facing extinction threats, identifying the relevance of natural mating patterns for conservation management.     

Stoichiometric impacts of increased carbon dioxide on a planktonic herbivore

The partial pressure of carbon dioxide (pCO₂) in lake ecosystems varies over four orders of magnitude and is affected by local and global environmental perturbations associated with both natural and anthropogenic processes. Little is known, however, about how changes in pCO₂ extend into the function and structure of food webs in freshwater ecosystems. To fill this gap, we performed laboratory experiments using the ecologically important planktonic herbivore Daphnia and its algal prey under a natural range of pCO₂ with low light and phosphorus supplies. The experiment showed that increased pCO₂ stimulated algal growth but reduced algal P : C ratio. When feeding on algae grown under high pCO₂, herbivore growth decreased regardless of algal abundance. Thus, high CO₂‐raised algae were poor food for Daphnia. Short‐term experimental supplementation of PO₄ raised the P content of the high CO₂‐raised algae and improved Daphnia growth, indicating that low Daphnia growth rates under high pCO₂ conditions were due to lowered P content in the algal food. These results suggest that, in freshwater ecosystems with low nutrient supplies, natural processes as well as anthropogenic perturbations resulting in increased pCO₂ enhance algal production but reduce energy and mass transfer efficiency to herbivores by decreasing algal nutritional quality.     

Trade‐offs and evolution of thermal adaptation in the Irish potato famine pathogen Phytophthora infestans

Temperature is one of the most important environmental parameters with crucial impacts on nearly all biological processes. Due to anthropogenic activity, average air temperatures are expected to increase by a few degrees in coming decades, accompanied by an increased occurrence of extreme temperature events. Such global trends are likely to have various major impacts on human society through their influence on natural ecosystems, food production and biotic interactions, including diseases. In this study, we used a combination of statistical genetics, experimental evolution and common garden experiments to investigate the evolutionary potential for thermal adaptation in the potato late blight pathogen, Phytophthora infestans, and infer its likely response to changing temperatures. We found a trade‐off associated with thermal adaptation to heterogeneous environments in P. infestans, with the degree of the trade‐off peaking approximately at the pathogen's optimum growth temperature. A genetic trade‐off in thermal adaptation was also evidenced by the negative association between a strain's growth rate and its thermal range for growth, and warm climates selecting for a low pathogen growth rate. We also found a mirror effect of phenotypic plasticity and genetic adaptation on growth rate. At below the optimum, phenotypic plasticity enhances pathogen's growth rate but nature selects for slower growing genotypes when temperature increases. At above the optimum, phenotypic plasticity reduces pathogen's growth rate but natural selection favours for faster growing genotypes when temperature increases further. We conclude from these findings that the growth rate of P. infestans will only be marginally affected by global warming.