Environmental gradients structure Daphnia pulex × pulicaria clonal distribution

The rarity of eukaryotic asexual reproduction is frequently attributed to the disadvantage of reduced genetic variation relative to sexual reproduction. However, parthenogenetic lineages that evolved repeatedly from sexual ancestors can generate regional pools of phenotypically diverse clones. Various theories to explain the maintenance of this genetic diversity as a result of environmental and spatial heterogeneity [frozen niche variation (FNV), general-purpose genotype] are conceptually similar to community ecological explanations for the maintenance of regional species diversity. We employed multivariate statistics common in community ecological research to study population genetic structure in the freshwater crustacean, Daphnia pulex × pulicaria. This parthenogenetic hybrid arose repeatedly from sexual ancestors. Daphnia pulex × pulicaria populations harboured substantial genetic variation among populations and the clonal composition at each pond corresponded to nutrient levels and invertebrate predator densities. The interclonal selection process described by the FNV hypothesis likely structured our D. pulex × pulicaria populations.     

Genetic composition of resident populations influences establishment success of immigrant species

We conducted an outdoor container experiment to test the hypothesis that the genetic composition of resident populations influences the establishment success of immigrant species. We manipulated the genetic compositions (source populations) of populations of the water flea Daphnia magna, a strong competitor in pond and shallow lake zooplankton communities, and monitored the establishment success of immigrant cladoceran species of a regional species pool. We show that establishment success is affected by the source population of the resident D. magna as well as by the presence/absence of macrophytes and the presence/absence of fish in the containers. Our results provide evidence that the genetic composition of resident populations can impact community assembly and metacommunity dynamics, and that community genetics can influence ecosystem functioning.     

Invasion of an asexual American water flea clone throughout Africa and rapid displacement of a native sibling species

The huge ecological and economic impact of biological invasions creates an urgent need for knowledge of traits that make invading species successful and factors helping indigenous populations to resist displacement by invading species or genotypes. High genetic diversity is generally considered to be advantageous in both processes. Combined with sex, it allows rapid evolution and adaptation to changing environments.We combined paleogenetic analysis with continent-wide survey of genetic diversity at nuclear and mitochondrial loci to reconstruct the invasion history of a single asexual American water flea clone (hybrid Daphnia pulexxDaphnia pulicaria) in Africa. Within 60 years of the original introduction of this invader, it displaced the genetically diverse, sexual population of native D. pulex in Lake Naivasha (Kenya), despite a formidable numerical advantage of the local population and continuous replenishment from a large dormant egg bank. Currently, the invading clone has spread throughout the range of native African D. pulex, where it appears to be the only occurring genotype.The absence of genetic variation did not hamper either the continent-wide establishment of this exotic lineage or the effective displacement of an indigenous and genetically diverse sibling species.     

Reticulate evolution of the Daphnia pulex complex as revealed by nuclear markers

The study of species complexes is of particular interest to understand how evolutionary young species maintain genomic integrity. The Daphnia pulex complex has been intensively studied as it includes species that dominate freshwater environments in the Northern hemisphere and as it is the sole North American complex that shows transitions to obligate parthenogenesis. Past studies using mitochondrial markers have revealed the presence of 10 distinct lineages in the complex. This study is the first to examine genetic relationships among seven species of the complex at nuclear markers (nine microsatellite loci and one protein-coding gene). Clones belonging to the seven species of the Daphnia pulex complex were characterized at the mitochondrial NADH dehydrogenase (ND5) gene and at the Lactate dehydrogenase (LDH) locus. K-means, principal coordinate analyses and phylogenetic network analyses on the microsatellite data all separated European D. pulicaria, D. tenebrosa, North American D. pulex, D. pulicaria and their hybrids into distinct clusters. The hybrid cluster was composed of diploid and polyploid hybrids with D. pulex mitochondria and some clones with D. pulicaria mitochondria. By contrast, the phylogeny of the D. pulex complex using Rab4 was not well resolved but still showed clusters consisting mostly of D. pulex alleles and others of D. pulicaria alleles. Incomplete lineage sorting and hybridization may obscure genetic relationships at this locus. This study shows that hybridization and introgression have played an important role in the evolution of this complex.     

Genome size evolution and polyploidy in the Daphnia pulex complex (Cladocera: Daphniidae)

Genome size was estimated in 49 clones of the Daphnia pulex complex from temperate and subarctic locations using flow cytometry and microsatellite DNA analyses. Significant genome size differences were found in diploid species belonging to the two genetically distinct groups (the pulicaria and the tenebrosa groups), with clones from the tenebrosa group having genome sizes 22% larger than those in the pulicaria group. Combined flow cytometry and microsatellite DNA analyses revealed that nearly all polyploid clones in the D. pulex complex are triploid and not tetraploid, as was previously suggested. Sequencing analyses of the ND5 gene to position clones in their respective clades within the D. pulex complex have uncovered three triploid clones of Daphnia middendorffiana with a D. pulex maternal parent. This result was unexpected because Daphnia pulicaria has always been identified as the maternal parent of these hybrid polyploid clones. Triploid clones likely owe their origins to interactions between sexual and asexual populations. Further interactions in the tenebrosa group have generated tetraploid clones but these events have been rare.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 68–79.     

Speciation with gene flow and the genetics of habitat transitions

Whether speciation can advance to completion in the face of initially high levels of gene flow is a very controversial topic in evolutionary biology. Extensive gene exchange is generally considered to homogenize populations and counteract divergence. Moreover, the role of introgressive hybridization in evolution remains largely unexplored in animals, particularly in freshwater zooplankton in which allopatric speciation is considered to be the norm. Our work investigates the genetic structure of two young ecological species: the pond species, Daphnia pulex and the lake species, Daphnia pulicaria. Phylogenetic and population genetics analyses were conducted on mitochondrial NADH dehydrogenase 5 (ND5) gene, the nuclear Lactate dehydrogenase (Ldh) gene and 21 nuclear microsatellite markers in 416 individuals from habitats with various degrees of permanence. The strong and consistent phylogenetic discordance between nuclear and mitochondrial markers suggests a complex evolutionary history of multiple independent habitat transition events that involved hybridization and introgression between lake and pond Daphnia. On the other hand, the low level of contemporary gene flow between adjacent populations indicates the presence of effective habitat isolating barriers. The Daphnia system provides strong evidence for a divergence-with-gene flow speciation model that involves multiple habitat transition events.     

Microsatellite variation in Daphnia pulex from both sides of the Baltic Sea

Despite large genetic differentiation among neighbouring populations of many freshwater zooplankton species, a macrogeographical homogeneity of allozyme variation is generally observed. A study on breeding systems in Scandinavian populations of Daphnia pulex suggested a latitudinally related cline in breeding system with both diploid cyclic parthenogens and diploid obligate parthenogens at the latitude of 60-61 degrees N. Variation at neutral markers may be more affected by selection at linked loci in such species than in strictly sexual species. In this paper I present a study of variation at five microsatellite loci in a total of 34 populations from small ponds and rockpools on both sides of the Baltic Sea at 60-61 degrees N. Two major groups, which may represent different species of the D. pulex complex, are defined with the microsatellites. Neighbouring populations show both similar and well differentiated genetic composition. Populations separated by larger geographical distances show only a large differentiation and a macrogeographic pattern. The large differentiation observed at small distances can be explained with small effective population size: variation at the microsatellite loci has been shaped by population bottlenecks followed with expansion in size, and possibly by selection. No conclusive evidence is found for obligative parthenogenesis.     

Invasibility of plankton food webs along a trophic state gradient

Biological invasions are becoming more common, yet the majority of introduced exotic species fail to establish viable populations in new environments. Current ecological research suggests that invasion success may be determined by properties of the native ecosystem, such as the supply rate of limiting nutrients (i.e. trophic state). We examined how trophic state influences invasion success by introducing an exotic zooplankter, Daphnia lumholtzi into native plankton communities in a series of experimental mesocosms exposed to a strong nutrient gradient. We predicted that the attributes of nutrient-enriched communities would increase the likelihood of a successful invasion attempt by D. lumholtzi . Contrary to our original predictions, we found that D. lumholtzi was often absent from mesocosms that developed under high nutrient supply rates. Instead, the presence of D. lumholtzi was associated with systems that had low nutrients, low zooplankton biomass, and high zooplankton species diversity. Using generalized estimating equations (GEE) and multivariate species data, we found that the presence–absence of D. lumholtzi could be explained by variations in zooplankton community structure, which was itself strongly influenced by nutrient supply rate. We argue that the apparent invasion success of D. lumholtzi was inhibited by the dominance of another cladoceran species, Chydorus sphaericus . These results suggest that the interaction between trophic state and species identity influenced the invasion success of introduced D. lumholtzi .     

Genetic diversity and genetic differentiation in Daphnia metapopulations with subpopulations of known age

If colonization of empty habitat patches causes genetic bottlenecks, freshly founded, young populations should be genetically less diverse than older ones that may have experienced successive rounds of immigration. This can be studied in metapopulations with subpopulations of known age. We studied allozyme variation in metapopulations of two species of water fleas (Daphnia) in the skerry archipelago of southern Finland. These populations have been monitored since 1982. Screening 49 populations of D. longispina and 77 populations of D. magna, separated by distances of 1.5-2180 m, we found that local genetic diversity increased with population age whereas pairwise differentiation among pools decreased with population age. These patterns persisted even after controlling for several potentially confounding ecological variables, indicating that extinction and recolonization dynamics decrease local genetic diversity and increase genetic differentiation in these metapopulations by causing genetic bottlenecks during colonization. We suggest that the effect of these bottlenecks may be twofold, namely decreasing genetic diversity by random sampling and leading to population-wide inbreeding. Subsequent immigration then may not only introduce new genetic material, but also lead to the production of noninbred hybrids, selection for which may cause immigrant alleles to increase in frequency, thus leading to increased genetic diversity in older populations.     

Predation and priority effects in experimental zooplankton communities

During colonization of new habitats, the sequence of arrival among species is in many cases determined by chance. Priority effects imply that differences in arrival time may lead to long-lasting differences in species dominance. To evaluate the importance of priority effects, we performed a community assembly experiment, manipulating the inoculation order of three large cladoceran zooplankton species. The inoculation treatments were crossed with a predation treatment to test whether the presence of a predator (larvae of the phantom midge Chaoborus ) results in changes in the strength of species sorting and priority effects. Our results clearly demonstrate priority effects, but also that the presence of a predator impacts both community assembly and the strength of priority effects. In the predation-free treatments, communities were dominated by either Daphnia magna or Daphnia obtusa , depending on the species arrival sequence. Whenever D. obtusa was inoculated after D. magna , the species displayed negative growth. In the presence of Chaoborus predation, the communities were generally dominated by the third species, Simocephalus vetulus . Here, the growth of D. magna was negative when the species was inoculated as second or third. Overall, our results underscore the importance of both priority effects and species sorting during community assembly.     

Phylogenetics and evolution of a circumarctic species complex (Gladocera: Daphnia pulex)

The evolutionary history of freshwater zooplankton is still relatively unknown. However, studies of the microcrustacean Daphnia have revealed interesting patterns; the daphniids that dominate ponds and lakes in the northern hemisphere may have recent origins, likely associated with the glacial advances and retreats during the Pleistocene. Moreover, they form species complexes that actively engage in hybridization and introgression. The present study examines the phylogenetic relationships among circumarctic members of the Daphnia pulex complex, through the analysis of sequence diversity in 498 nt of the ND5 mitochondrial gene. Our results suggest that the complex is composed of three major clades, two of which are subdivided into at least eight different lineages. Clearly, species in the complex show genetic discontinuity. Many lineages originated during the Pleistocene, but at least three lineages diverged during the Pliocene. Two taxa ( D. pulex, D. pulicaria ), thought to be broadly distributed in the northern hemisphere, are shown to be endemic to single continents. In general, the diversification of the pulex complex is characterized by rapidly dispersed lineages spanning enormous distances and also by endemism in temperate areas. Gene flow among lineages from the temperate region of different continents are restricted to rare intercontinental migrations across a polar bridge followed by convergent morphological evolution.     

Long-term dynamics in rock pool Daphnia metapopulations

Metapopulations of Daphnia longispina , D. magna and D. pulex on 16 islands containing 507 rock pools were studied over 17 yr (autumns 1982–1998). Two yearly samples were taken representing early and late summer conditions. A local extinction was assumed when a species was absent from a pool for more than one year. Average yearly extinction rates, calculated from probability of survival in age grouped data, were close to 20%, and number of extinctions was on average balanced by the number of colonizations. Extinction rates during the first year following colonization were 45–50% in all species, but later decreased to low values. In first-year data, single species populations of D. magna had lower extinction rates than in multi-species pools. In later years all species combinations had similar extinction rates. The average proportion of rock pools occupied by D. longispina in any given year was 0.178, by D. magna 0.169 and by D. pulex 0.056. In 22% of cases, coexistence was observed. 71% of the pools were colonized at least once. The distribution of shortest colonization distances was left-skewed, and median distances (7–8 m) were same in all species. The distribution of colonizations mostly corresponded to the expected frequencies calculated as the product of frequencies of source and target pools. Both D. longispina and D. magna colonized pools already occupied with a somewhat higher probability than empty pools. Probably owing to variation of habitat quality, Daphnia populations in some rock pools appear to be less prone to extinction, providing sources of dispersal to patches with higher extinction risk. The system appears to be at an approximate equilibrium, with several characteristics close to classical metapopulation system.     

Cryptic intercontinental colonization in water fleas Daphnia pulicaria inferred from phylogenetic analysis of mitochondrial DNA variation

The water fleas of the Daphnia pulex complex play a key role in freshwater ecosystems throughout the northern hemisphere. Despite the fact that they have been the subject of study for numerous biological disciplines, their phylogeny and species delimitation remain controversial. We used DNA sequence variation of the mitochondrial ND5 gene to reconstruct the phylogenetic relationships of D. pulicaria Forbes, a widespread member of this complex from North America and Europe. Populations from the two continents respectively split into two evolutionary lineages, Eastern Nearctic and European, which each belong to another main clade within the D. pulex complex (the pulicaria and tenebrosa groups, respectively). Unexpectedly, melanin and carotenoid pigmented D. pulicaria populations from European high-mountain lakes were not allied with the transparent populations inhabiting the same lakes and the lowland ponds and reservoirs throughout Europe, but were included with the samples from Canada and Greenland in the Eastern Nearctic lineage. Until now populations belonging to this lineage were known only from Canada and North Atlantic islands, but not from mainland Europe. Independent data from microsatellite markers supported the genetic distinctiveness of the sympatric carotenoid pigmented and transparent populations and suggested that they may have undergone transition to obligate parthenogenesis, possibly as a consequence of past introgressive hybridization. Two different taxa are therefore confused under the name D. pulicaria in Europe. The close phylogenetic relationships of European populations with those from Canada and Greenland suggest that the Nearctic lineage is of recent origin in Europe via intercontinental dispersal from the North America. It has evolved melanin and carotenoid pigmentation as adaptations against the UV light stress, which enable it to share habitat occupied by the transparent European species. The Nearctic D. pulicaria thus provides a new model for studying successful intercontinental invasion. In general, our study demonstrates that a considerable part of the diversity among widespread taxa of cladoceran crustaceans has been overlooked in morphological taxonomies.     

PATTERNS OF GENETIC ARCHITECTURE FOR LIFE-HISTORY TRAITS AND MOLECULAR MARKERS IN A SUBDIVIDED SPECIES

Abstract Understanding the utility and limitations of molecular markers for predicting the evolutionary potential of natural populations is important for both evolutionary and conservation genetics. To address this issue, the distribution of genetic variation for quantitative traits and molecular markers is estimated within and among 14 permanent lake populations of Daphnia pulicaria representing two regional groups from Oregon. Estimates of population subdivision for molecular and quantitative traits are concordant, with Q _ST generally exceeding G _ST. There is no evidence that microsatellites loci are less informative about subdivision for quantitative traits than are allozyme loci. Character-specific comparison of Q _ST and G _ST support divergent selection pressures among populations for the majority of life-history traits in both coast and mountain regions. The level of within-population variation for molecular markers is uninformative as to the genetic variation maintained for quantitative traits. In D. pulicaria , regional differences in the frequency of sex may contribute to variation in the maintenance of expressed within-population quantitative-genetic variation without substantially impacting diversity at the genic level. These data are compared to an identical dataset for 17 populations of the temporary-pond species, D. pulex .     

Long-term impact of an invertebrate predator, Heterocope septentrionalis, on an arctic pond zooplankton community

1. A long-term field experiment to determine what forces structure and maintain the large-bodied zooplankton assemblages in ponds which lack visual predators was undertaken at the Toolik Lake Research Station in arctic Alaska. Predatory copepods, Heterocope septentrionalis, were introduced to a pond that lacked both fish and invertebrate predators, but contained small- to medium-sized zooplankton, Bosmina longirostris , Daphnia pulex , and Diaptomus pribilofensis. A second pond, which also lacked any predators but had a population of B. longirostris , but no other abundant species, served as a reference population for B. longirostris.
2. The introduction of H. septentrionalis caused the extinction of D. pulex within 1 year and drove B. longirostris to extremely low densities within 4 years. The population of B. longirostris in the reference pond fluctuated throughout the study period, but remained above five individuals per litre. This experiment demonstrates that H. septentrionalis , under natural conditions, made a numerical response to abundant prey and had the capacity to eliminate or reduce vulnerable prey populations of small- to medium-sized zooplankton.     

Effects of predation by Chaoborus flavicans on crustacean zooplankton of Lake Lenore, Washington

1. After Chaoborus flavicans became established in 1974, the species composition of zooplankton in Lake Lenore changed. Diaptomus nevadensis disappeared and densities of Diaptomus sicilis were reduced.
2. A transplant experiment showed the D. nevadensis could survive in Lake Lenore water in the absence of Chaoborus . The disappearance of D. nevadensis was probably a consequence of Chaoborus predation.
3. Although densities of Daphnia pulicaria † were similar before and after the colonization of C. flavicans , juvenile D. pulicaria began producing neck-teeth during the first summer Chaoborus was present.
4. The seasonal pattern of neck-teeth production by juvenile D. pilicaria did not correlate with density of Chaoborus but rather with a combination of water temperature and Chaoborus density, suggesting that metabolic processes are a component of induction of neck-teeth in this species.     

Acidification and the structure of crustacean zooplankton in mountain lakes: The Tatra Mountains (Slovakia,Poland)

Species composition of planktonic Crustacea in 102 lakes in the West and High Tatra Mountains, studied during the peak of anthropogenic acidification (1978–1996), is presented in this work. Zooplankton of the Tatra lakes have been studied since the middle of the 19^th century, which later enabled the recognition of lake acidification and the assessment of its effect on the plankton community of lake ecosystems. In the pre-acidification period, the distribution of zooplankton was determined namely by the lake altitude and orientation (north vs. south) and by the catchment character. Crustacean zooplankton in larger lakes consisted of a limited number of species, with Acanthodiaptomus denticornis and Daphnia longispina dominating lakes in the forest zone, and Arctodiaptomus alpinus, Cyclops abyssorum, Daphnia longispina, Daphnia pulicaria, and Holopedium gibberum dominating lakes in the alpine zone. Ceriodaphnia quadrangula, Daphnia obtusa, Daphnia pulex, and Mixodiaptomus tatricus occurred in lakes with high concentrations of dissolved organic matter and in strongly acidified waters. Anthropogenic acidification has caused drastic changes in both the chemistry and biology of the Tatra lakes. Based on their status during the acidification peak, lakes were divided into three categories: non-acidified (with no change in the species composition of crustacean zooplankton due to the acidification), acidified (planktonic Crustacea disappeared in lakes with meadow-rocky catchments), and strongly acidified lakes where original Crustacea in meadow-rocky catchment lakes disappeared and were replaced by populations of the acid-tolerant littoral species Acanthocyclops vernalis, Chydorus sphaericus, and Eucyclops serrulatus. The acidification-induced processes of oligotrophication and toxicity of aluminium played a key role in the extinction of species. Despite the first signs of biological recovery observed in the early 2000s, acidification remains the most important factor governing the structure of plankton in the Tatra lakes.     

Propagule pressure and native community connectivity interact to influence invasion success in metacommunities

Mechanistic insights from invasion biology indicate that propagule pressure of exotic species and native community structure can independently influence establishment success. The role of native community connectivity via species dispersal and its potential interaction with propagule pressure on invasion success in metacommunities, however, remains unknown. Native community connectivity may increase biotic resistance to invasion by enhancing species richness and evenness, but the effects could depend upon the level of propagule pressure. In this study, a mesocosm experiment was used to evaluate the independent and combined effects of exotic propagule pressure and native community connectivity on invasion success. The effects of three levels of exotic Daphnia lumholtzi propagule pressure on establishment success, community structure and ecosystem attributes were evaluated in native zooplankton communities connected by species dispersal versus unconnected communities, and relative to a control without native species. Establishment of the exotic species exhibited a propagule dose‐dependent relationship with high levels of propagule pressure resulting in the greatest establishment success. Native community connectivity, however, effectively reduced establishment at the low level of propagule pressure and further augmented native species richness across propagule pressure treatments. Propagule pressure largely determined the negative impacts of the exotic species on native species richness, native biomass and edible producer biomass. The results highlight that native community connectivity can reduce invasion success at a low propagule dose and decrease extinction risk of native competitors, but high propagule pressure can overcome connectivity‐mediated biotic resistance to influence establishment and impact of the exotic species. Together, the results emphasize the importance of the interaction of propagule pressure and community connectivity as a regulator of invasion success, and argue for the maintenance of metacommunity connectivity to confer invasion resistance.     

Food web structure provides biotic resistance against plankton invasion attempts

It is generally accepted that native communities provide resistance against invaders through biotic interactions. However, much remains uncertain about the types of ecological processes and community attributes that contribute to biotic resistance. We used experimental mesocosms to examine how zooplankton community structure, invertebrate predation, and nutrient supply jointly affected the establishment of the exotic Daphnia lumholtzi. We predicted that establishment would increase with declining biomass and diversity of native zooplankton communities and that an invertebrate predator (IP) would indirectly facilitate the establishment of D. lumholtzi due to its relatively long predator-deterring spines. Furthermore, we hypothesized that elevated nutrient supply would increase algal food availability and facilitate establishment. Only when the biomass and diversity of native zooplankton were significantly reduced, was D.␣lumholtzi able to successfully invade mesocosms. Although invertebrate predation and resource supply modified attributes of native zooplankton communities, they did not influence the establishment of D. lumholtzi. Overall, our␣results are consistent with observed population dynamics in invaded reservoirs where D.␣lumholtzi tends to be present only during the late summer, coinciding with historic mid-summer declines in native zooplankton populations. Lakes and reservoirs may be more susceptible to invasion not only by D. lumholtzi, but also by other planktonic species, in the late summer when native communities exhibit characteristics associated with lower levels of biotic resistance.