Lowered female reproductive effort as an indicator for increased male production and sexuality in Daphnia (Crustacea: Cladocera)

Summary

The relationship between environmental factors, sex ratio, mode of reproduction, and female reproductive effort was examined in the cyclically parthenogenetic Daphnia magna. Female reproductive effort was found to decline before a significant production of males and sexual eggs takes place. Unlike factors such as crowding, poor nourishment, low (sometimes high) temperature and short or long day length, lowered reproductive effort is not a cue but rather an indicator of the selective advantage that would accrue from a changed sex ratio and mode of reproduction. The mechanism of the complex system of environmental sex determination in Daphnia is reviewed, and the adaptivity of ESD is discussed.     

Obligate asex in a rotifer and the role of sexual signals

Transitions to asexuality have occurred in many animals and plants, yet the biological mechanisms causing such transitions have often remained unclear. Cyclical parthenogens, such as cladocerans, rotifers or aphids often give rise to obligate asexual lineages. In many rotifers, chemical signals that accumulate during population crowding trigger the induction of sexual stages. In this study, I tested two hypotheses on the origin of obligate parthenogenesis in the rotifer Brachionus calyciflorus: (i) that obligate parthenogens have lost the responsiveness to the sexual signal; and (ii) that obligate parthenogens have lost the ability to produce the sexual signal. Pairwise cross-induction assays among three obligate parthenogenetic strains and two cyclically parthenogenetic (sexual) strains were used to test these hypotheses. I found that obligate parthenogens can induce sexual reproduction in sexual strains, but not vice versa. This demonstrates that obligate parthenogens do still produce the sexual signal, but have lost responsiveness to that signal.     

Male offspring production by asexual Potamopyrgus antipodarum, a New Zealand snail

As only females contribute directly to population growth, sexual females investing equally in sons and daughters experience a two-fold cost relative to asexuals producing only daughters. Typically, researchers have focused on benefits of sex that can counter this 'cost of males' and thus explain its predominance. Here, we instead ask whether asexuals might also pay a cost of males by quantifying the rate of son production in 45 experimental populations ('lineages') founded by obligately asexual female Potamopyrgus antipodarum. This New Zealand snail is a powerful model for studying sex because phenotypically similar sexual and asexual forms often coexist, allowing direct comparisons between sexuals and asexuals. After 2 years of culture, 23 of the 45 lineages had produced males, demonstrating that asexual P. antipodarum can make sons. We used maximum-likelihood analysis of a model of male production in which only some lineages can produce males to estimate that ~50% of lineages have the ability to produce males and that ~5% of the offspring of male-producing lineages are male. Lineages producing males in the first year of the experiment were more likely to make males in the second, suggesting that some asexual lineages might pay a cost of males relative to other asexual lineages. Finally, we used a simple deterministic model of population dynamics to evaluate how male production affects the rate of invasion of an asexual lineage into a sexual population, and found that the estimated rate of male production by asexual P. antipodarum is too low to influence invasion dynamics.     

Evidence for widespread cryptic sexual generations in apparently purely asexual Andricus gallwasps

Oak gallwasps (Hymenoptera, Cynipidae, Cynipini) are one of seven major animal taxa that commonly reproduce by cyclical parthenogenesis (CP). A major question in research on CP taxa is the frequency with which lineages lose their sexual generations, and diversify as purely asexual radiations. Most oak gallwasp species are only known from an asexual generation, and secondary loss of sex has been conclusively demonstrated in several species, particularly members of the holarctic genus Andricus. This raises the possibility of widespread secondary loss of sex in the Cynipini, and of diversification within purely parthenogenetic lineages. We use two approaches based on analyses of allele frequency data to test for cryptic sexual generations in eight apparently asexual European species distributed through a major western palaearctic lineage of the gallwasp genus Andricus. All species showing adequate levels of polymorphism (7/8) showed signatures of sex compatible with cyclical parthenogenesis. We also use DNA sequence data to test the hypothesis that ignorance of these sexual generations (despite extensive study on this group) results from failure to discriminate among known but morphologically indistinguishable sexual generations. This hypothesis is supported: 35 sequences attributed by leading cynipid taxonomists to a single sexual adult morphospecies, Andricus burgundus, were found to represent the sexual generations of at least six Andricus species. We confirm cryptic sexual generations in a total of 11 Andricus species, suggesting that secondary loss of sex is rare in Andricus.     

Clonal diversity,clonal persistence and rapid taxon replacement in natural populations of species and hybrids of the Daphnia longispina complex

Hybridization is common among cyclical parthenogens, especially in zooplankton species assemblages of the genus Daphnia. To explore hybridization dynamics and the extent of clonal diversity in the Daphnia longispina complex, we analysed population structure in eight permanent lakes. Based on 15 microsatellite loci, three major taxonomic units emerged: two species, D. galeata and D. longispina and their F1 hybrids, supported by factorial correspondence analysis and two Bayesian methods. At the same time, the detection of backcross classes differed between methods. Mean clonal diversity was lowest in the F1 hybrids, as expected from the high rate of asexual reproduction. Within taxa, replicated genotypes were of clonal origin, but clonal lineages persisted in subsequent years in only one of three resampled lakes. In another lake, the taxon composition changed from being dominated by hybrids to complete dominance by one parental taxon. Such a year‐to‐year taxon replacement has not been reported for the D. longispina complex before. Our data on this hybrid complex illustrate that high‐resolution genotyping is essential for the understanding of ecological and evolutionary outcomes of hybridization in partially clonal taxa.     

Spatial and temporal escape from fungal parasitism in natural communities of anciently asexual bdelloid rotifers

Sexual reproduction is costly, but it is nearly ubiquitous among plants and animals, whereas obligately asexual taxa are rare and almost always short-lived. The Red Queen hypothesis proposes that sex overcomes its costs by enabling organisms to keep pace with coevolving parasites and pathogens. If so, the few cases of stable long-term asexuality ought to be found in groups whose coevolutionary interactions with parasites are unusually weak. In theory, antagonistic coevolution will be attenuated if hosts disperse among patches within a metapopulation separately from parasites and more rapidly. We examined whether these conditions are met in natural communities of bdelloid rotifers, one of the longest-lived asexual lineages. At any life stage, these microscopic invertebrates can tolerate the complete desiccation of their ephemeral freshwater habitats, surviving as dormant propagules that are readily carried by the wind. In our field experiments, desiccation and wind transport enabled bdelloids to disperse independently of multiple fungal parasites, in both time and space. Surveys of bdelloid communities in unmanipulated moss patches confirmed that fungal parasitism was negatively correlated with extended drought and increasing height (exposure to wind). Bdelloid ecology therefore matches a key condition of models in which asexuals persist through spatio-temporal decoupling from coevolving enemies.     

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.     

Why is sex so rare in Lecane inermis (Rotifera: Monogononta) in wastewater treatment plants?

The monogonont rotifer Lecane inermis is commonly known as a facultative parthenogen. Unexpectedly, among numerous lineages we isolated from wastewater treatment plants (WWTP), only one was capable of sexual reproduction. We investigated why sex was so rare among L. inermis in WWTP. The reproductive modes of lineages derived from the sexual lineage were examined. Among all lineages, the fraction of those reproducing only asexually for 14 d was 0.39. In the subsequent round, the fraction of asexual lineages reached 0.61. The population growth rate of the parthenogenetic lineages was significantly higher than that of the sexual lineages. We simulated the fate of rotifer populations in WWTP by removing 10% of the experimental cultures each day. After 10 d of these conditions, the mean number of females was greater in parthenogenetic than in sexual lineages. After 20 d, only solitary dormant eggs remained in the sexual lineages. It therefore appears that the loss of sex may be attributed to the specific conditions of the WWTP. When there is no risk of desiccation and no need for dormancy, the fast‐growing parthenogens outcompete lineages investing in costly sex. Furthermore, even if some resting eggs were deposited, they would be washed out from the system with the excess sludge.     

Reproductive mode and population genetic structure of the cereal aphid Sitobion avenae studied using phenotypic and microsatellite markers

As French populations of the aphid Sitobion avenae exhibit a range of reproductive modes, this species provides a good opportunity for studying the evolution of breeding system variation. The present analysis combined ecological and genetic investigations into the spatial distribution of variation in reproductive mode. Reproductive mode was characterized in 277 lineages of S. avenae from France, and these aphids were scored for five microsatellite loci. The analyses revealed strong geographical partitioning of breeding systems, with obligate asexuals mostly restricted to the south of France, while lineages producing sexual forms were more common in the north. Contrary to what might be anticipated for organisms with frequent parthenogenesis, there was substantial genic and genotypic diversity, even in the obligately asexual lineages. More than 120 different genotypes were detected among the 277 aphid lineages, with an average of 5.9 alleles per locus (range four to 16) and heterozygosity of 56.7%. As with previous studies of allozyme variation in aphids, most loci showed heterozygote deficits, and disequilibrium was common among allelic variants at different loci, even after removal of replicate copies of genotypes that might have been derived through clonal reproduction. Our results suggest that selection is important in structuring reproductive systems and genetic variation in French S. avenae. Canonical correspondence analysis was employed to examine the associations between genotypic and phenotypic variables, enabling the identification of alleles correlated with life-history traits.     

A high incidence of parthenogenesis in agricultural pests

Parthenogenetic species are assumed to represent evolutionary dead ends, yet parthenogenesis is common in some groups of invertebrates particularly in those found in relatively constant environments. This suggests that parthenogenetic reproduction might be common in pest invertebrates from uniform agricultural environments. Based on the evaluations of two databases from North America and Italy, we found that parthenogenetic species comprised 45 per cent (North America) or 48 per cent (Italy) of pest species derived from genera where parthenogenesis occurred, compared with an overall incidence of 10 per cent or 16 per cent in these genera. In establishing these patterns, we included only genera containing at least some member species that reproduced by parthenogenesis. The high incidence of parthenogenesis in pest species is spread across different families and several insect orders. Parthenogenetic reproduction may be favoured in agricultural environments when particular clones have a high fitness across multiple generations. Increasing the complexity and variability of agricultural environments represents one way of potentially controlling parthenogenetic pest species.