Morphological Similarity and Ecological Overlap in Two Rotifer Species
Co-occurrence of cryptic species raises theoretically relevant questions regarding their coexistence and ecological similarity. Given their great morphological similitude and close phylogenetic relationship (i.e., niche retention), these species will have similar ecological requirements and are expected to have strong competitive interactions. This raises the problem of finding the mechanisms that may explain the coexistence of cryptic species and challenges the conventional view of coexistence based on niche differentiation. The cryptic species complex of the rotifer Brachionus plicatilis is an excellent model to study these questions and to test hypotheses regarding ecological differentia…
Does haplodiploidy purge inbreeding depression in rotifer populations?
Background Inbreeding depression is an important evolutionary factor, particularly when new habitats are colonized by few individuals. Then, inbreeding depression by drift could favour the establishment of later immigrants because their hybrid offspring would enjoy higher fitness. Rotifers are the only major zooplanktonic group where information on inbreeding depression is still critically scarce, despite the fact that in cyclical parthenogenetic rotifers males are haploid and could purge deleterious recessive alleles, thereby decreasing inbreeding depression. Methodology/Principal Findings We studied the effects of inbreeding in two populations of the cyclical parthenogenetic rotifer Brach…
Effects of population outcrossing on rotifer fitness
Abstract Background Outcrossing between populations can exert either positive or negative effects on offspring fitness. Cyclically parthenogenetic rotifers, like other continental zooplankters, show high genetic differentiation despite their high potential for passive dispersal. Within this context, the effects of outcrossing may be relevant in modulating gene flow between populations through selection for or against interpopulation hybrids. Nevertheless, these effects remain practically unexplored in rotifers. Here, the consequences of outcrossing on the rotifer Brachionus plicatilis were investigated. Cross-mating experiments were performed between a reference population and three alterna…
Resource competition between sympatric sibling rotifer species
Mechanisms underlying competitive interactions are important in understanding the structure of planktonic communities, particularly the coexistence of similar species. Here we present experimental results of exploitative competition among three sympatric sibling species of the Brachionus plicatilis complex for two differently-sized species of food microalgae. These three rotifer species are to be found in seasonal succession in brackish ponds on the Spanish Mediterranean coast; they can, however, co-occur for long periods. The functional and numerical responses of the three Brachionus species to both food microalgae, although similar, differed. Neither rotifer population growth nor grazing …
Modes, mechanisms and evidence of bet hedging in rotifer diapause traits
In this contribution, we review our knowledge on bet-hedging strategies associated with rotifer diapause. First, we describe the ecological scenario under which bet hedging is likely to have evolved in three diapause-related traits in monogonont rotifer populations: (1) the timing of sex (because diapausing eggs are produced via sexual reproduction), (2) the sexual reproduction ratio (i.e. the fraction of sexually reproducing females) and (3) the timing of diapausing egg hatching. Then, we describe how to discriminate among bet-hedging modes and discuss which modes and mechanisms better fit the variability observed in these traits in rotifers. Finally, we evaluate the strength of the empiri…
Allocation patterns in modes of reproduction in two facultatively sexual cryptic rotifer species
Many zooplankters rely on diapausing stages to survive unsuitable conditions in time-varying habitats. In facultativesexualrotifers, reproductive effortallocatedtothe sexuallyproduced diapausingeggs isat the expenseofthe subitaneousparthenogenetic eggs, generatingatrade-offbetweencurrentand future population growth.Thetimingand the amountof sex (the sexual pattern) affect diapausing-egg production. This switch to sex is complex because the reproductivemode is separated in distinct females: asexual (female-producing), unfertilized sexual (male-producing) and fertilizedsexual (diapause-egg-producing). We studied sexual patterns and life-history variation of these females in two crypticspecies…
A simple model relating habitat features to a diapause egg bank
As a way to escape from adverse conditions, many zooplankton populations produce diapausing eggs that accumulate in the sediments and hatch when suitable environmental conditions are restored. While buried in the sediment, diapausing eggs may be affected by several processes (i.e., production, hatching, deterioration, and loss). We present a simple mathematical model for the dynamics of diapausing eggs in the sediment. We were mainly inspired by the model organism Brachionus plicatilis, a cyclical parthenogen rotifer, but the model is applicable to other zooplankters. Three diapausing egg categories are used as variables in our model: (1) healthy-looking eggs, assumed to represent the fract…
Hatching and viability of rotifer diapausing eggs collected from pond sediments
SUMMARY 1. Planktonic rotifers inhabiting variable environments produce diapausing eggs that accumulate in the sediment of lakes and ponds, forming egg banks that may withstand adverse periods. A common assumption in zooplankton diapausing egg bank studies is to count as viable all eggs in the sediment that look healthy. This assumption should be challenged by asking how effectively ‘healthy-looking’ eggs represent viable eggs. 2. In this study, viability of more than 1100 ‘healthy-looking’ diapausing eggs belonging to the Brachionus plicatilis species complex was assessed in a laboratory hatching experiment. Eggs were collected at different depths from sediment cores obtained from 15 ponds…
Protein patterns in rotifers: the timing of aging
Single rotifer individuals have been characterized biochemically to obtain a fingerprint of their physiological state using a modified ultrasensitive silver-stain procedure to detect total proteins in polyacrylamide gels. Patterns are completely uniform for young isogenic individuals raised in the same culture, but they start to change when these individuals reach a certain age. This age is close to the mean lifespan and to both the cessation of body growth and reproduction. Variability is greatest among individuals of the same chronological age, thus the rate of aging is different even among individuals having identical genotypes and experiencing the same environment.
Selection on life-history traits and genetic population divergence in rotifers
A combination of founder effects and local adaptation – the Monopolization hypothesis – has been proposed to reconcile the strong population differentiation of zooplankton dwelling in ponds and lakes and their high dispersal abilities. The role genetic drift plays in genetic differentiation of zooplankton is well documented, but the impact of natural selection has received less attention. Here, we compare differentiation in neutral genetic markers (FST) and in quantitative traits (QST) in six natural populations of the rotifer Brachionus plicatilis to assess the importance of natural selection in explaining genetic differentiation of life-history traits. Five life-history traits were measur…
Review paper: Ecological genetics of Brachionus sympatric sibling species
In this paper we review previous studies on sympatric Brachionus populations in Torreblanca Marsh as a model of evolutionary and ecological relationships between closely related species. The marsh is a wetland on the Mediterranean coast of Spain with high spatial and temporal heterogeneity. Allozyme and morphometric analysis showed that Brachionus group plicatilis (formerly, Brachionus plicatilis and currently split into B. plicatilis and B. rotundiformis) was composed of three groups of genotypes with no evidence of gene flow between them (B. plicatilis, B. rotundiformis SM and B. rotundiformis SS). Correlations between seasonal and spatial distributions, on one hand, and temperature and s…
Widespread secondary contact and new glacial refugia in the halophilic rotifer Brachionus plicatilis in the Iberian Peninsula.
Small aquatic organisms harbour deep phylogeographic patterns and highly structured populations even at local scales. These patterns indicate restricted gene flow, despite these organisms' high dispersal abilities, and have been explained by a combination of (1) strong founder effects due to rapidly growing populations and very large population sizes, and (2) the development of diapausing egg banks and local adaptation, resulting in low effective gene flow, what is known as the Monopolization hypothesis. In this study, we build up on our understanding of the mitochondrial phylogeography of the halophilic rotifer Brachionus plicatilis in the Iberian Peninsula by both increasing the number of…
Predation as a factor mediating resource competition among rotifer sibling species
The relevance of predation as a factor mediating the competitive interaction among ecologically very similar species is investigated by experimentally analyzing the effect of the copepod predator Diacyclops bicuspidatus odessanus on three sibling rotifer species belonging to the Brachionus plicatilis species complex. These rotifer species are similar in shape but show notable differences in body size. Predator and prey species co-occur in brackish waterbodies close to the Mediterranean coast of Spain. First, we characterized differential vulnerability of rotifers to predation. A consistent tendency of higher predation rates on smaller prey (i.e., smaller species and younger individuals) was…
Sex Allocation in Haplodiploid Cyclical Parthenogens with Density‐Dependent Proportion of Males
Departament de Microbiologia i Ecologia, Universitat de Birky and Gilbert 1971; Wallace and Snell 1991), which Valencia, E46100-Burjassot (Valencia), Spain includes an asexual (amictic) and a sexual (mictic) phase, the diapausing form being the sexually produced resting Submitted September 22, 1997; Accepted April 21, 1998 egg. Habitat colonization begins when the resting eggs hatch and emerge from the sediments. With these hatchlings, the amictic phase starts, which is a repeated sequence of amictic females parthenogenetically produc
Survival analysis of three clones of Brachionus plicatilis (Rotifera)
Age-specific survival schedules of females from three genetically different clones of Brachionus plicatilis were analyzed at several environmental conditions in the laboratory.
Mixis strategies and resting eeg production of rotifers living in temporally-varying habitats
A dynamic model based on six differential equations has been developed to explore the control of mixis of rotifers living in temporally-varying habitats. The equations give variation rates of amictic females, three stages of mictic females, males and resting eggs. The model takes into account some constraints on mixis (e.g., male-female encounter probability and effort involved in resting egg production) and its predictions have been generated by computer simulation using parameter values from the literature. For simulation, a time-dependent birth rate function was assumed to account for changes in the environment, and several mixis patterns (i.e., moment of mixis induction and mictic rate …
Surface glycoproteins in copepods: potential signals for mate recognition
The mechanism male copepods use to recognize mates is not well understood. Both chemical and mechanical cues have been implicated, but the relative importance of these is not known. This lack of knowledge is despite the belief that mate recognition has a critical role in maintaining reproductive isolation of many species and influences the direction of evolution. Glycoproteins are used as mating signals by a number of aquatic organisms including rotifers, ciliates, and algae. We have developed techniques for selectively probing surface glycoproteins in zooplankton using fluorescently labeled lectins. We examined surface glycoproteins on the urosomes of several species of marine and freshwat…
Genomic signatures of local adaptation to the degree of environmental predictability in rotifers
AbstractEnvironmental fluctuations are ubiquitous and thus essential for the study of adaptation. Despite this, genome evolution in response to environmental fluctuations —and more specifically to the degree of environmental predictability– is still unknown. Saline lakes in the Mediterranean region are remarkably diverse in their ecological conditions, which can lead to divergent local adaptation patterns in the inhabiting aquatic organisms. The facultatively sexual rotifer Brachionus plicatilis shows diverging local adaptation in its life-history traits in relation to estimated environmental predictability in its habitats. Here, we used an integrative approach —combining environmental, phe…
Relationships between mixis in Brachionus plicatilis and preconditioning of culture medium by crowding
Several experiments with Brachionus plicatilis have been conducted to test the existence of chemical-mediated induction of mixis. In a first experimental set, bioassays were used to test relationships between preconditioning of culture medium to high population density and the occurrence of mixis in mass cultures with these media. The results show that a preconditioned medium has inducing properties that are comparable to the crowding effect.
Comparative toxicant sensitivity of sexual and asexual reproduction in the rotiferBrachionus calyciflorus
Cyclically parthenogenetic zooplankters like rotifers are important tools for assessing toxicity in aquatic environments. Sexual reproduction is an essential component of rotifer life cycles, but current toxicity tests utilize only asexual reproduction. The authors compared the effects of four toxicants on asexual and sexual reproduction of the rotifer Brachionus calyciflorus. Toxicants had a differential effect on sexual and asexual reproduction, with sexual reproduction consistently the most sensitive. Concentrations of 0.2 {mu}g/ml PCP (sodium pentachlorophenate) had no effect on the asexual reproductive rate, but significantly reduced sexual reproduction. Likewise, chlorpyrifos concentr…
Life-history variation, environmental fluctuations and competition in ecologically similar species: modeling the case of rotifers
Competition for resources can lead to species exclusion. However, this exclusion may be avoided if species show differential adaptation to physical environment. Empirical studies on competition are difficult when species are phylogenetically close and have complex life cycles. This is the case of B. plicatilis and B. manjavacas, two cryptic rotifer species differing in their salinity niches and in life-history traits related to sex and diapause. These differences have been suggested to promote the stable co-occurrence observed in natural populations of these species. However, in a previous empirical study, the outcome of competition between both species was always exclusion. Here, we theore…
Gene expression in diapausing rotifer eggs in response to divergent environmental predictability regimes
AbstractIn unpredictable environments in which reliable cues for predicting environmental variation are lacking, a diversifying bet-hedging strategy for diapause exit is expected to evolve, whereby only a portion of diapausing forms will resume development at the first occurrence of suitable conditions. This study focused on diapause termination in the rotifer Brachionus plicatilis s.s., addressing the transcriptional profile of diapausing eggs from environments differing in the level of predictability and the relationship of such profiles with hatching patterns. RNA-Seq analyses revealed significant differences in gene expression between diapausing eggs produced in the laboratory under com…
Variability for mixis initiation in Brachionus plicatilis
Deductions from both evolutionary models and inductive argumentation from empirical data support the notion of intraspecific variability for the initiation of sexual reproduction (mixis) within rotifer populations. In this study, we focus on the time and density at which mixis is initiated in a growing population. Cyclical parthenogenetic clones of Brachionus plicatilis established by hatching of resting eggs, isolated from a natural habitat, have been tested at the start of their sexual phase. Clones exhibited great variation for this trait, their time of switching to sexual reproduction being correlated with population density. Most of the variation for mixis initiation has either low or …
Selection of low investment in sex in a cyclically parthenogenetic rotifer
Cyclical parthenogens, which combine asexual and sexual reproduction, are good models for research into the ecological and population processes affecting the evolutionary maintenance of sex. Sex in cyclically parthenogenetic rotifers is necessary for diapausing egg production, which is essential to survive adverse conditions between planktonic growing seasons. However, within a planktonic season sexual reproduction prevents clonal proliferation. Hence, clones with a low propensity for sex should be selected, becoming dominant in the population as the growing season progresses. In this context, we studied the dynamics of the heritable variation in propensity for sexual reproduction among clo…
When to be sexual: sex allocation theory and population density-dependent induction of sex in cyclical parthenogens
The timing of sex is a critical fitness component in the cyclically parthenogenetic life-cycle of rotifers. It has been hypothesized that sex in rotifers is optimally timed to high population density because male‐female encounters are more probable. Because sexual females produce either males or, if inseminated, diapausing eggs, the advantage of a higher male‐female encounter rate is that allocation to male production can be lower. This is paradoxical in the context of the sex allocation theory developed for rotifers, as the theory predicts equal numbers of male-producing and diapausing-egg producing females. We investigated this paradox using both empirical data and theoretical analysis. L…
Quantifying unpredictability: A multiple-model approach based on satellite imagery data from Mediterranean ponds.
Fluctuations in environmental parameters are increasingly being recognized as essential features of any habitat. The quantification of whether environmental fluctuations are prevalently predictable or unpredictable is remarkably relevant to understanding the evolutionary responses of organisms. However, when characterizing the relevant features of natural habitats, ecologists typically face two problems: (1) gathering long-term data and (2) handling the hard-won data. This paper takes advantage of the free access to long-term recordings of remote sensing data (27 years, Landsat TM/ETM+) to assess a set of environmental models for estimating environmental predictability. The case study inclu…
Patterns in rotifer diapausing egg banks: Density and viability
Here we present a quantitative study on the density, age and viability of the diapausing egg banks of the rotifer species complex Brachionus plicatilis in the sediments of 15 water bodies from Eastern Spain. Sampled ponds, located in coastal and inland areas, varied in salinity and ranged in size, depth and permanence. By identifying ‘hatched’, ‘deteriorated’ and ‘viable’ diapausing eggs in the sediment samples, we estimated production, hatching and deterioration in relation to the habitat properties of each pond. Our results indicate the presence of large numbers of diapausing eggs in the sediments of almost all of the ponds studied (2–115 eggs cm −2 ). Inland ponds tended to have higher d…
Mictic patterns of the rotifer Brachionus plicatilis Müller in small ponds
Populations of the rotifer Brachionus plicatilis were monitored in three small ponds in a marsh on the Mediterranean coast. Samples were taken approximately every three weeks from July 1992 to November 1993. Salinity, temperature, conductivity, pH and oxygen concentration were measured in the field. Population density was determined from preserved quantitative samples. Individuals were classified as mictic females, amictic females, non-ovigerous females, and males, differentiating between two morphotypes (‘S’ and ‘L’). From these counts, a level of mixis was calculated. We also determined the proportion of mictic females in natural populations by culturing females isolated from fresh sample…
Crossed induction of sex in sympatric congeneric rotifer populations
The transition from asexual to sexual reproduction in rotifers of the genus Brachionus (Monogononta) is triggered by a chemical signal produced and released by the rotifers themselves; the signal accumulates in the environment as population density increases. The response to this signal has been hypothesized to be speciesspecific. If not, the timing of sex and final diapausing egg production of a species might not be optimized. In this study, a set of experiments—based on individual and mass culture approaches—was carried out to investigate the differentiation in sex induction signals between sympatric and allopatric congeneric Brachionus populations by analyzing the capability of the mediu…
Measuring the potential for growth in populations investing in diapause
AbstractThe intrinsic rate of population increase (r) is a common performance measure in many ecological and evolutionary studies. However, in life cycles with diapause investment resources are split into a short-term (current population growth) and a long-term (population survival through periods of unsuitable habitat conditions) component, which complicates the use of r as a single performance measure. Here we propose a new measure that integrates both performance components into a single parameter, the potential intrinsic growth rate, rpot. This is the rate of increase that a population/genotype would have if no investment in diapausing stages would occur. We show that rpot can be comput…
Deterioration patterns in diapausing egg banks of Brachionus (Müller, 1786) rotifer species
Rotifers are cyclical parthenogens that produce sexual diapausing eggs at some stage in their life cycle. These eggs are encysted embryos that remain viable for extended periods in lake and pond sediments, thus acting as an egg bank with many ecological and evolutionary consequences. Despite its importance to rotifer evolution, there are no studies on resting egg deterioration and associated processes in natural environments. In this study, more than 4000 diapausing eggs of species from the Brachionus plicatilis complex, which includes several closely related cryptic species, were collected from different sediment depths in 15 ponds in eastern Spain and were classified according to three fe…
Life-history traits, abiotic environment and coexistence: The case of two cryptic rotifer species
Abstract Trade-offs are important in life-history evolution and coexistence of competitors. However, how alternative life-history optima might promote competitor coexistence has received little attention. The rotifers Brachionus plicatilis and Brachionus manjavacas are two cryptic species with a considerable ecological overlap in relation to biotic factors. These species often co-occur in temporal brackish ponds characterised by environmental fluctuations. In these rotifers, sexual reproduction results in diapausing stages, which are able to survive through adverse conditions but constrain current population growth. In the present work, the differential responses of both cryptic rotifer spe…
Evidence for an even sex allocation in haplodiploid cyclical parthenogens
Recent theoretical work has shown that haplodiploid cyclical parthenogens, such as rotifers, are expected to have an equal frequency of male-producing and resting-egg producing females during their sexual phase. We tested this prediction by following sexual reproduction dynamics in two laboratory populations and one field population of the rotifer Brachionus plicatilis through two growing seasons. We recorded population density, proportion of sexual females, and sex allocation (the proportion of male-producing sexual females as a fraction of total sexual females). We found this sex allocation ratio to vary from 0.3 to 1.0 in single sampling events. However, when we computed sex allocation b…
Bet-hedging in diapausing egg hatching of temporary rotifer populations - A review of models and new insights
Habitat unpredictability is a local adaptation factor shaping life-history traits in rotifer populations. It may select for the evolution of bet-hedging through risk-spreading strategies in diapausing egg hatching. This means that a fraction of diapausing eggs in wild populations do not hatch even when the conditions are favorable for population growth. Thus, there is a remaining fraction of viable diapausing eggs standing in the sediments for longer periods. According to theory, it is expected that the incidence of bet-hedging strategies for diapausing egg hatching will be higher in more uncertain habitats. Here, we review the major predictions derived from theoretical models applied to th…
Adaptation in response to environmental unpredictability
Understanding how organisms adaptively respond to environmental fluctuations is a fundamental question in evolutionary biology. The Mediterranean region typically exhibits levels of environmental unpredictability that vary greatly in habitats over small geographical scales. In cyclically parthenogenetic rotifers, clonal proliferation occurs along with occasional bouts of sex. These bouts contribute to the production of diapausing eggs, which allows survival between growing seasons. Here, we studied two diapause-related traits in rotifers using clones from nine Brachionus plicatilis natural populations that vary in the degree of environmental unpredictability. We tested the hypothesis that …
Long-term competitive dynamics of two cryptic rotifer species: diapause and fluctuating conditions.
Life-history traits may have an important role in promoting species coexistence. However, the complexity of certain life cycles makes it difficult to draw conclusions about the conditions for coexistence or exclusion based on the study of short-term competitive dynamics. Brachionus plicatilis and B. manjavacasare two cryptic rotifer species co-occurring in many lakes on the Iberian Peninsula. They have a complex life cycle in which cyclical parthenogenesis occurs with diapausing stages being the result of sexual reproduction. B. plicatilis and B. manjavacasare identical in morphology and size, their biotic niches are broadly overlapping, and they have similar competitive abilities. However,…
Ecological genomics of adaptation to unpredictability in experimental rotifer populations
AbstractElucidating the genetic basis of phenotypic variation in response to different environments is key to understanding how populations evolve. Facultatively sexual rotifers can develop adaptive responses to fluctuating environments. In a previous evolution experiment, diapause-related traits changed rapidly in response to two selective regimes (predictable vs unpredictable) in laboratory populations of the rotifer Brachionus plicatilis. Here, we investigate the genomic basis of adaptation to environmental unpredictability in these experimental populations. We identified and genotyped genome-wide polymorphisms in 169 clones from both selective regimes after seven cycles of selection usi…
Data from: Adaptation in response to environmental unpredictability
Understanding how organisms adaptively respond to environmental fluctuations is a fundamental question in evolutionary biology. The Mediterranean region typically exhibits levels of environmental unpredictability that vary greatly in habitats over small geographical scales. In cyclically parthenogenetic rotifers, clonal proliferation occurs along with occasional bouts of sex. These bouts contribute to the production of diapausing eggs, which allows survival between growing seasons. Here, we studied two diapause-related traits in rotifers using clones from nine Brachionus plicatilis natural populations that vary in the degree of environmental unpredictability. We tested the hypothesis that t…