Lawrence J. Weider

Lake ecosystems: Rapid evolution revealed by dormant eggs

Natural selection can lead to rapid changes in organisms, which can in turn influence ecosystem processes. A key factor in the functioning of lake ecosystems is the rate at which primary producers are eaten, and major consumers, such as the zooplankton Daphnia, can be subject to strong selection pressures when phytoplankton assemblages change. Lake Constance in central Europe experienced a period of eutrophication (the biological effects of an input of plant nutrients) during the 1960s–70s, which caused an increase in the abundance of nutritionally poor or even toxic cyanobacteria. By hatching long-dormant eggs of Daphnia galeata found in lake sediments, we show that the mean resistance of Daphnia genotypes to dietary cyanobacteria increased significantly during this eutrophication. This rapid evolution of resistance has implications for the ways that ecosystems respond to nutrient enrichment through the impact of grazers on primary production.

NATURAL SELECTION FOR GRAZER RESISTANCE TO TOXIC CYANOBACTERIA: EVOLUTION OF PHENOTYPIC PLASTICITY?

Abstract We studied the selection response of the freshwater grazing zooplankter, Daphnia galeata, to increased abundance of cyanobacteria in its environment. Cyanobacteria are a poor‐quality and often toxic food. Distinct genotypes of D. galeata were hatched from diapausing eggs extracted from three time horizons in the sediments of Lake Constance, Europe, covering the period 1962 to 1997, a time of change in both the prevalence of planktonic cyanobacteria and levels of phosphorus pollution. We assessed whether the grazers evolved to become more resistant to dietary cyanobacteria by exposing genetically distinct clones to two diets, one composed only of the nutritious green alga, Scenedesmus obliquus (good food), and the other a mixture of S. obliquus and the toxic cyanobacterium Microcystis aeruginosa (poor food). Genotype performance was measured as the specific rate of weight gain from neonate to maturity (gj).

CLONAL-DIVERSITY PATTERNS AND BREEDING-SYSTEM VARIATION IN DAPHNIA PULEX, AN ASEXUAL-SEXUAL COMPLEX

Some individuals of the cladoceran crustacean, Daphnia pulex, reproduce by cyclic parthenogenesis, while others are obligate parthenogens. Cyclic parthenogenesis is the primitive breeding system; the transition to obligate parthenogenesis has been linked to sex‐limited meiosis‐suppression. Detailed study of patterns of breeding‐system distribution and clonal diversity is justified because D. pulex is the first species in which the loss of sex has been related to this mechanism. The present study investigated the genotypic characteristics of 10 D. pulex populations from each of 22 sites in the Great Lakes watershed. This analysis revealed that populations reproducing by cyclic parthenogenesis were uncommon and restricted to southern sites. Most populations reproduced by obligate parthenogenesis, with the electrophoretic survey revealing an average of three clones per pond and 145 unique clones over the watershed. A combinatorial analysis was used to examine the relationships between clone discovery in the asexual populations and both sample size and genetic‐sampling intensity. This analysis showed that the few clones found in individual ponds were readily discriminated, while diversity on a regional scale was underestimated. These methods provide a quantitative basis for assessing the level of clonal diversity in asexual populations and in asexually transmitted segments of the genome.

Plasticity of Daphnia life histories in response to chemical cues from predators

The possible induction of life-history shifts in prey by chemicals released into the environment by potential predators was examined. Laboratory life-table experiments were conducted to examine the influence of chemical substances released from vertebrate (fish) and invertebrate (Notonectidae) predators on life-history features of two clones (B―coexists with fish, W―from a fishless pond) of the freshwater cladoceran crustacean, Daphnia magna. Significant differences between treatments in key life-history features (i.e. size and age at first reproduction) were detected for each clone. Both clones showed a significantly smaller size at first reproduction when raised under fish-treated water, when compared with animals raised under invertebrate-treated water

Long–term genetic shifts in a microcrustacean egg bank associated with anthropogenic changes in the Lake Constance ecosystem

Diapausing egg banks of aquatic zooplankton have the potential to remain viable for decades or even centuries, and can thus harbour potentially high levels of genetic variation. Diapausing (ephippial) eggs from the Daphnia galeata–hyalina complex (Crustacea: Anomopoda) in Lake Constance (Bodensee), Germany, were isolated from sections of dated sediment cores, hatched in the laboratory, and established as a clone bank. We used cellulose acetate electrophoresis at four polymorphic enzyme loci (Pgm, Pgi, Ao, and Got) to examine long–term temporal changes in the genetic composition of the hatchling pool. Our results indicate that significant shifts have occurred in the genetic structure of this population, which parallel concomitant shifts in the trophic state of Lake Constance during the past 25–35 years. Here we discuss the utility of egg bank propagules as good model organisms to study microevolution, as related to past environmental change.

Differential response of Daphnia genotypes to oxygen stress: respiration rates, hemoglobin content and low-oxygen tolerance

SummaryLaboratory respiration rate experiments using three electrophoretically identified clones of the fresh water, planktonic cladoceran, Daphnia pulex, from an eutrophic farm pond, indicated that clones acclimated to both low and high oxygen levels, regulated oxygen consumption across a wide range of oxygen concentrations (1.0–9.0 mg· liter-1). A “threshold” oxygen level of 0.5–1.0 mg·liter-1 was reached, where animals succumbed to oxygen stress, regardless of hemoglobin content. No significant clonal differences in respiration rates were found. These data suggest that members of this Daphnia population are able to regulate oxygen metabolism across a wide range of ambient oxygen concentrations, and indicate a well-adapted respiratory system.Low-oxygen tolerance experiments and hemoglobin measurements indicated further that physiological differences indeed exist between clones; one clone produced the lowest amount of hemoglobin and was least tolerant of low oxygen levels. These data imply that spatial and temporal changes in dissolved oxygen concentration may be an important selective force influencing the clonal (genotypic) composition of natural cladoceran populations.

HOLARCTIC PHYLOGEOGRAPHY OF AN ASEXUAL SPECIES COMPLEX I. MITOCHONDRIAL DNA VARIATION IN ARCTIC DAPHNIA

Pleistocene glacial cycles undoubtedly altered the evolutionary trajectories of many taxa, yet few studies have examined the impact of such events on genetic differentiation and phylogeography at large geographic scales. Here we present the results of a circumarctic survey of mitochondrial DNA diversity in members of the Daphnia pulex complex. The analysis involved the survey of restriction site polymorphisms in a 2100‐bp fragment of the NADH‐4 (ND4) and NADH‐5 (ND5) genes for 276 populations representing the two major groups (tenebrosa and pulicaria) in this complex across their Holarctic range. A comparison of the distribution patterns for seven clades in this complex revealed very clear phylogeographic structuring. Most notably, pulicaria group lineages were restricted primarily to the Nearctic, with some colonization of formerly glaciated portions of northern Europe. This group was not detected from vast expanses of northern Eurasia, including the Beringian glacial refuge. In contrast, tenebrosa group haplotypes showed considerable intercontinental divergence between Eurasian and North American lineages, but were absent from Greenland and Iceland, as well as the Canadian arctic archipelago. Dispersal in Eurasia was primarily in a westerly direction from Beringia, whereas dispersal in the Nearctic followed proglacial drainage patterns. Long‐distance dispersal of certain lineages was observed in both groups, and variation in haplotype richness and nucleotide diversity allowed us to make inferences about the positioning of putative glacial refugia. Overall, the phylogeographic pattern of diversification in this arctic complex is characterized by the apparently unique postglacial histories for each clade, indicating that even closely allied taxa can respond independently to the allopatric effects of glacial cycles. This is in sharp contrast to other phylogeographic studies of species assemblages from more southern (unglaciated) latitudes, which are often characterized by concordant patterns.

Glacial refugia, haplotype distributions, and clonal richness of the Daphnia pulex complex in arctic Canada

As part of a large international Arctic biodiversity expedition (Tundra Northwest ′99), we examined the distribution of members of the arctic Daphnia pulex complex (Cladocera, Anomopoda) from 121 tundra ponds, spread across 16 sites spanning a large portion of arctic Canada (i.e. from 62°22′ N to 79°01′ N; 66°45′ W to 139°37′ W). Using allozyme electrophoresis and mitochondrial (mt)DNA analyses, we examined the population genetic (clonal) structure of these populations. The following taxa were detected in this complex: Daphnia pulicaria, D. middendorffiana and D. tenebrosa. Clear geographical differences in mean clonal richness and diversity were observed, with most western sites exhibiting higher clonal richness and diversity, than sites in the eastern Canadian Arctic. For both the pulicaria group (i.e. D. pulicaria and D. middendorffiana) and D. tenebrosa, the highest mean regional clonal richness was detected from the southern section of Banks Island, an unglaciated site situated on the edge or directly in the eastern fringe of the Beringian glacial refuge. A significant negative correlation was found between geographical distance from the Beringian edge, and overall regional clonal richness (i.e. sites closer to the edge harboured greater clonal richness). These results clearly indicate that more recently deglaciated regions (i.e. eastern Canadian Arctic) harbour lower levels of clonal richness than western regions nearer Beringia. We discuss the role that glacial refugia have played in influencing both biotic and genetic diversity in arctic taxa.

Functional and ecological significance of rDNA intergenic spacer variation in a clonal organism under divergent selection for production rate

It has recently been hypothesized that variation in the intergenic spacer (IGS) of rDNA has considerable developmental, evolutionary and ecological significance through effects on growth rate and body C : N : P stoichiometry resulting from the role of the IGS in production of rRNA. To test these ideas, we assessed changes in size and structure of the repetitive region of the IGS, juvenile growth rate (JGR), RNA and phosphorus (P) contents in clonal lineages of Daphnia pulex derived from a single female and subjected to divergent selection on weight–specific fecundity (WSF). As a result of selection, WSF diverged rapidly, with significant reductions within two generations. Other significant changes accompanying shifts in WSF were that juveniles produced by low–WSF females grew more rapidly and had higher RNA and P contents. An increased predominance of long IGS variants was observed in lineages with elevated JGRs and low WSF. The observed variations in IGS length were related to the number of subrepeat units carrying a promoter sequence in the repetitive region. These results strongly support the hypothesized relationships, indicate a genetic mechanism for the evolution of such associations and demonstrate that Daphnia (and perhaps other parthenogens) possess considerable potential for rapid adaptive change in major life–history traits.

Genome streamlining and the elemental costs of growth

Pervasive relationships between growth rate, genome size and RNA content exist. One interesting potential consequence of these interrelationships is that selection for high growth rate should be associated with small genomes and high RNA content. Here, we use phosphorus (P) and nitrogen (N) demands of growth along with nucleic acid production as the currency to explore the interrelationships between growth rate and genome size in eukaryotes. We argue that reallocation of P (and eventually N) from DNA to RNA under sustained selection for rapid growth in nutritionally limited environments can lead to genome streamlining in eukaryotes, and that this mechanism might contribute to the evolution of reduced genome size.