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…

Ageing via perception costs of reproduction magnifies sexual selection.

Understanding what factors modulate sexual selection intensity is crucial to a wide variety of evolutionary processes. Recent studies show that perception of sex pheromones can severely impact male mortality when it is not followed by mating (perception costs of reproduction). Here, we examine the idea that this may magnify sexual selection by further decreasing the fitness of males with inherently low mating success, hence increasing the opportunity for sexual selection. We use mathematical modelling to show that even modest mortality perception costs can significantly increase variability in male reproductive success under a wide range of demographic conditions. We then conduct a series …

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…

Ageing via sexual perception is a by-product of male adaptive plasticity inDrosophila melanogaster

ABSTRACTSensory perception of environmental cues can dramatically modulate ageing across distant taxa. For example, maleDrosophila melanogasterage faster if they perceive female cues but fail to mate (ageing via sexual perception). This finding has been a breakthrough for our understanding of the mechanisms of ageing, yet we ignore how and why such responses have evolved. Here, we usedD. melanogasterto ask whether ageing via sexual perception may be a by-product of plastic adaptive responses to female cues, and found that while long-term sexual perception leads to reproductive costs, short-term perception increases male lifetime reproductive success in a competitive environment. Simulations…

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…

Density-dependent regulation of natural and laboratory rotifer populations

Density-dependent regulation of abundance is fundamentally important in the dynamics of most animal populations. Density effects, however, have rarely been quantified in natural populations, so population models typically have a large uncertainty in their predictions. We used models generated from time series analysis to explore the form and strength of density-dependence in several natural rotifer populations. Population growth rate (r) decreased linearly or non-linearly with increased population density, depending on the rotifer species. Density effects in natural populations reduced r to 0 at densities of 1–101−1 for 8 of the 9 rotifer species investigated. The sensitivities of these spe…

Species size affects hatching response to different temperature regimes in a rotifer cryptic species complex

The strategy of decreasing size with increasing temperature known as Bergmann’s rule operates at geographic scale and in spite of extensive studies still presents a puzzle to researches. The aim of this work was to verify whether patterns of diapausing egg hatching of closely related species are consistent with the expectations from Bergmann’s rule. In a laboratory study of the cryptic species complex of the rotifer Brachionus plicatilis, the response to temperature (17.5, 22.5, and 25.0 °C) of diapausing eggs collected in a pond where the three tested species coexist was assessed by (1) the number of hatchlings emerging or (2) the time needed to hatch. Our results show that the response to…

The effect of environmental uncertainty and diapause investment on the occurrence of specialist and generalist species

The evolution of specialist and generalist strategies is a central topic in ecology with strong implications for the biodiversity and structure of communities. Environmental unpredictability has been suggested as a key factor affecting the relative advantages of generalist species. However, life cycle features, like diapause, can also play a major role in the competitive dynamics between generalists and specialists. Zooplanktonic communities of continental waters are suitable models to study this; they inhabit water bodies that vary temporally with different degrees of uncertainty and rely on the production of diapause stages to survive across the year. We developed a simple theoretical mod…

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…

Size variation in Brachionus plicatilis resting eggs

The effect of temperature and salinity on resting egg size of two Brachionus plicatilis (Rotifera) clones was investigated. Clones were selected according to their different behaviour in laying resting eggs: one clone ejects them, whereas they remain inside the females body in the other clone. The difference in resting eggs size between the two clones is noticeable, although the difference is not as great as that between female body size. An important temperature-salinity interaction on resting egg size has been observed. The general inverse relationship between size and temperature is only true at lower temperatures. At high temperatures size varies around the mean although could be greate…

Electronic Supplementary File from Ageing via perception costs of reproduction magnifies sexual selection

Contains supplementary figures and tables referred to in the manuscript.

Speciation in the Brachionus plicatilis Species Complex

The Brachionus plicatilis species complex is the best-studied example among rotifers where the use of integrative taxonomy, coupling morphology, ecology, physiology, cross-mating experiments, and DNA taxonomy helps disentangling the biological reality of the different species in the complex. Here we review the theoretical and empirical approaches in species definition applied to the B. plicatilis complex, we outline the history of the discovery of the complex, and we explore the evidence in support of the currently accepted presence of 15 species. We review the evidence for long-distance dispersal and for co-occurrence of the species in the complex, including the processes favoring the co-o…

On the taxonomy of three sympatric sibling species of the Brachionus plicatilis (Rotifera) complex from Spain, with the description of B. ibericus n. sp.

The accumulation of evidence during the last decade led to the splitting of the Brachionus plicatilis complex (Rotifera) into two morphologically recognizable species: B. plicatilis Muller and B. rotundiformis Tschugunoff, previously referred to as L- and S-type B. plicatilis (s.l.), respectively. However, recent population genetics and molecular studies have revealed that each of these taxa concern cryptic species complexes. In particular, in Torreblanca Marsh, a wetland on the Mediterranean coast of Spain, three genetically distinct groups in this rotifer complex have been shown to co-occur. Differences in genetic markers, ecological preferences, mixis responses, mating behaviour and no e…

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.

Biometric analysis of Brachionus plicatilis ecotypes from Spanish lagoons

Univariate comparisons and several multivariate statistical analyses have been performed to study the morphometric variability of B. plicatilis. Both laboratory clones kept under constant conditions and natural populations from different Spanish lagoons and different times of the year have been compared. The results show that not only size, but also allometric coefficients are influenced by environmental factors. However, an important genetic component in the variation of shape and size has been visualized. A clear North-South ordination of the populations of the different lagoons and an important dispersion between their summer populations as well as great differences due to seasonal varia…

Founder effects drive the genetic structure of passively dispersed aquatic invertebrates

Populations of passively dispersed organisms in continental aquatic habitats typically show high levels of neutral genetic differentiation, despite their high dispersal capabilities. Several evolutionary factors, including founder events and local adaptation, and life cycle features such as high population growth rates and the presence of propagule banks, have been proposed to be responsible for this paradox. Here, we have modeled the colonization process in these organisms to assess the impact of migration rate, growth rate, population size, local adaptation and life-cycle features on their population genetic structure. Our simulation results show that the strongest effect on population st…

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…

Coexistence of cryptic rotifer species: ecological and genetic characterisation of Brachionus plicatilis

SUMMARY 1. The coexistence of five cryptic species of the rotifer species complex Brachionus plicatilis was investigated in four coastal Mediterranean ponds. Monthly sampling was undertaken for 15 months and species were characterised using allozyme electrophoresis. 2. We describe species-diagnostic allozyme loci that can be used for rapid identification of these species. 3. The five species overlapped to some extent in their temporal use of the ponds, although some seasonal segregation was observed. 4. The match between temporal and spatial distribution and limnological conditions suggested ecological specialisation in some cases, although we found striking examples of extensive seasonal o…

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…

Fifteen species in one: deciphering the Brachionus plicatilis species complex (Rotifera, Monogononta) through DNA taxonomy

Understanding patterns and processes in biological diversity is a critical task given current and rapid environmental change. Such knowledge is even more essential when the taxa under consideration are important ecological and evolutionary models. One of these cases is the monogonont rotifer cryptic species complex Brachionus plicatilis, which is by far the most extensively studied group of rotifers, is widely used in aquaculture, and is known to host a large amount of unresolved diversity. Here we collate a dataset of previously available and newly generated sequences of COI and ITS1 for 1273 isolates of the B. plicatilis complex and apply three approaches in DNA taxonomy (i.e. ABGD, PTP, …

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…

Small, beautiful and sexy: what rotifers tell us about ecology and evolution

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…

Ecological genetics of a cyclical parthenogen in temporary habitats

Populations of the rotifer Brachionus plicatilis inhabiting three temporary ponds in Torreblanca Marsh (Castellon, Spain) were regularly screened for allozyme variation, sexual reproduction levels and population densities during an annual cycle. Relevant ecological parameters in the ponds were also recorded. The electrophoretic survey of the three ponds (Poza Sur, Poza Norte and Canal Central) revealed a high level of overall genetic polymorphism in four marker loci, but only 13 multilocus genotypes were found. We classified clones into three clonal groups (SS, SM, L) characterized by unique arrays of alleles in the four marker loci, and significant differences in body shape and size. Clona…

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 …

Using probability of extinction to evaluate the ecological significance of toxicant effects

A large component of uncertainty in ecological risk assessment (ERA) arises from the disparity between the time scale of toxicity measurements and the time scale of predictions of ERA models. It is difficult to make predictions about the persistence of populations from data from short-term toxicity tests. Reproductive toxicity tests provide data about how population growth rate (r) is reduced with toxicant exposure. Although reduction in r is believed to be one of the most important effects of toxicant exposure, its ecological significance has been difficult to quantify. For rotifers, r is typically reduced by 10 to 15% at no-observed-effect concentrations (NOEC). We investigated r reductio…

Relationships between oxygen concentration and patterns of energy metabolism in the rotifer Brachionus plicatilis

Abstract 1. 1. Activities of 10 enzymes and accumulation of two metabolites under experimental hypoxia were investigated in the rotifer Brachionus plicatilis . 2. 2. Pyruvate kinase (PK), lactate dehydrogenase (LDH), malic enzyme (ME), phosphoenolpyruvate carboxykinase (PEPCK), malate dehydrogenase (MDH) and fumarase (FUM) activities showed great increase at low oxygen levels. Alcohol dehydrogenase (ADH) activity was not detected. 3. 3. Alanine concentration showed an increase with low oxygen concentrations, while alanine aminotransferase (GTP) showed a slight activity increase with oxygen levels. The high alanine concentration was interpreted as enhanced proteolysis. 4. 4. Our results show…

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.

Evolutionary dynamics of ‘the’ bdelloid and monogonont rotifer life-history patterns

Substantial differences in both life-table characteristics and reproductive patterns distinguish bdelloid from monogonont rotifers. Bdelloids reproduce only asexually, whereas most monogononts are cyclical parthenogens. We explore some of the adaptive consequences of these life-history differences using a computer model to simulate the evolutionary acquisition of new beneficial mutations. A one-locus mutation-selection regime based on the life-history characteristics of bdelloids indicates that asexuals can maintain higher levels of both allelic and genotypic diversity over a longer time period than obligate sexuals. These results are produced by differences in the magnitude of random genet…

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…

Sex Loss in Monogonont Rotifers

Monogonont rotifers are small, aquatic invertebrates capable of asexual and sexual reproduction. Sexual reproduction is required to produce diapausing eggs, which are able to survive adverse periods that typically occur every year. Their cyclically parthenogenetic life-cycle is believed to retain the advantages of recombination while minimizing the cost of sex. However, this life cycle is also thought to be unstable due to periodic loss of sexual reproduction by directional selection. Explaining the evolutionary dynamics of the monogonont rotifer life cycle is important for understanding how cyclical parthenogenesis is maintained, and for comparing monogononts with their close relatives, th…

Diapause as escape strategy to exposure to toxicants: response of Brachionus calyciforus to arsenic

Invertebrate organisms commonly respond to environmental fluctuation by entering diapause. Production of diapause in monogonont rotifers involves a previous switch from asexual to partial sexual reproduction. Although zooplankton have been used in ecotoxicological assays, often their true vulnerability to toxicants is underestimated by not incorporating the sexual phase. We experimentally analyzed traits involved in sexual reproduction and diapause in the cyclically parthenogenetic freshwater rotifer, Brachionus calyciflorus, exposed to arsenic, a metalloid naturally found in high concentrations in desert zones, focusing on the effectiveness of diapause as an escape response in the face of …

Why are male rotifers dwarf?

Morphological stasis of two species belonging to the L-morphotype in the Brachionus plicatilis species complex

Detection and characterization of sibling species complexes in zooplankton are critical to understanding their ecological responses and patterns of evolution. The taxon Brachionus plicatilis is a complex of at least 14 species with three major, deeply diverged clades, which are morphologically distinct. We studied morphometric differences between two species — B. plicatilis sensu stricto and B. ‘Manjavacas’ — which belong to the L-(large) morphotype and often co-occur in ponds or lakes. B. plicatilis s.s. was on average 6% longer than B. ‘Manjavacas’. They differed significantly in the measurements related to lorica spines. A significant discriminant function relating spine measurements was…

Persistent genetic signatures of colonization inBrachionus manjavacasrotifers in the Iberian Peninsula

Recent phylogeographical assessments have consistently shown that continental zooplankton display high levels of population subdivision, despite the high dispersal capacity of their diapausing propagules. As such, there is an apparent paradox between observed cosmopolitanism in the zooplankton that is associated with long-distance dispersal, and strong phylogeographical structures at a regional scale. Such population dynamics, far from migration-drift equilibrium, have been shown in the rotifer species complex Brachionus plicatilis, a group of over a dozen species inhabiting salt lakes and coastal lagoons worldwide. Here we present the mitochondrial DNA phylogeography of one of these specie…

Predatory interactions between a cyclopoid copepod and three sibling rotifer species

SUMMARY 1. Cyclopoid copepod predation on rotifers affects the dynamics and structure of zooplankton communities. We address the differential vulnerability of three sympatric rotifer sibling species belonging to the Brachionus plicatilis species complex. These co-occur with their cyclopoid predator, Diacyclops bicuspidatus odessanus. 2. Using video recording and tracking, we analysed the steps in predation including attack distance, attack angle, and rotifer species swimming in the presence and absence of the predator. Our results show the greater vulnerability of B. rotundiformis (the smallest species) to D. b. odessanus predation, which is associated with a high percentage of attacks afte…

Life-cycle switching and coexistence of species with no niche differentiation.

The increasing evidence of coexistence of cryptic species with no recognized niche differentiation has called attention to mechanisms reducing competition that are not based on niche-differentiation. Only sex-based mechanisms have been shown to create the negative feedback needed for stable coexistence of competitors with completely overlapping niches. Here we show that density-dependent sexual and diapause investment can mediate coexistence of facultative sexual species having identical niches. We modelled the dynamics of two competing cyclical parthenogens with species-specific density-dependent sexual and diapause investment and either equal or different competitive abilities. We show th…

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…

Selective feeding of Arctodiaptomus salinus (Copepoda, Calanoida) on co-occurring sibling rotifer species

Summary 1. Using two- and three-dimensional video recordings, we examined the steps involved in predation that lead to the differential vulnerability of three sympatric rotifer sibling species (Brachionus plicatilis, B. ibericus and B. rotundiformis) to a co-occurring, predatory, calanoid copepod (Arctodiaptomus salinus). 2. Brachionus rotundiformis, the smallest prey tested, was the most vulnerable with the highest encounter rate, probability of attack, capture and ingestion, and the lowest handling time. 3. Comparison of our results with those of a previous study shows that A. salinus is a more efficient predator than a co-occurring cyclopoid copepod (Diacyclops bicuspidatus odessanus) fe…

Review paper: Seasonal variation as a determinant of population structure in rotifers reproducing by cyclical parthenogenesis

Monogonont rotifers live in habitats that display extensively variation in both biotic and abiotic components. Much of this variation is seasonal and therefore predictable for a given pond or lake. In 1972, King proposed one physiological and two genetic models presenting alternative modes of adaptation to this temporal variation. Our purpose in the present paper is to review and evaluate how our knowledge of the seasonal structure of rotifer populations has changed in the past 25 years. Seasonal changes in clone frequencies have been reported from three studies of natural populations using electrophoretic analysis of isozymes. In one of these studies there was evidence for substantial temp…

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…

Long-Term Coexistence of Rotifer Cryptic Species

Despite their high morphological similarity, cryptic species often coexist in aquatic habitats presenting a challenge in the framework of niche differentiation theory and coexistence mechanisms. Here we use a rotifer species complex inhabiting highly unpredictable and fluctuating salt lakes to gain insights into the mechanisms involved in stable coexistence in cryptic species. We combined molecular barcoding surveys of planktonic populations and paleogenetic analysis of diapausing eggs to reconstruct the current and historical coexistence dynamics of two highly morphologically similar rotifer species, B. plicatilis and B. manjavacas. In addition, we carried out laboratory experiments using …

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…

Body size variability across habitats in the Brachionus plicatilis cryptic species complex

AbstractThe body size response to temperature is one of the most recognizable but still poorly understood ecological phenomena. Other covarying environmental factors are frequently invoked as either affecting the strength of that response or even driving this pattern. We tested the body size response in five species representing the Brachionus plicatilis cryptic species complex, inhabiting 10 brackish ponds with different environmental characteristics. Principal Component Analysis selected salinity and oxygen concentration as the most important factors, while temperature and pH were less influential in explaining variation of limnological parameters. Path analysis showed a positive interclo…

Distribution of Brachionus species in Spanish mediterranean wetlands

In this study 200 zooplankton samples were Burjassotcollected (1979–1980), from 57 different wetlands in coastal Mediterranean Spain (CMS) and examined for the occurrence of Brachionus species. Data on 17 separate physical and chemical features of these water bodies were obtained from samples collected at the same time. Ten different Brachionus species were found in these wetlands, but only six occurred frequently enough to allow further examination of their distributional patterns using multivariate discriminant analysis. To separate these species, three analyses were performed using the 17 physical and chemical parameters, or their ratios. Three discriminant functions accounted for 80% or…

Empirical evidence for fast temperature-dependent body size evolution in rotifers

Organisms tend to decrease in size with increasing temperature by phenotypic plasticity (the temperature-size rule; ectotherms) and/or genetically (Bergmann’s rule; all organisms). In this study, the evolutionary response of body size to temperature was examined in the cyclically parthenogenetic rotifer Brachionus plicatilis. Our aim was to investigate whether this species, already known to decrease in size with increasing temperature by phenotypic plasticity, presents a similar pattern at the genetic level. We exposed a multiclonal mixture of B. plicatilis to experimental evolution at low and high temperature and monitored body size weekly. Within a month, we observed a smaller size at hig…

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 …

Speciation in monogonont rotifers

Monogonont rotifers are cyclical parthenogens livingin limnic habitats with considerable seasonalvariation and often with island-like features. Theoccurrence of bisexual reproduction in these organismsmakes it feasible to define ’fields for generecombination‘, i.e. biological species. In thispaper, we analyze the structure of the diversity inmonogonont rotifers using several data sets: taxonomicand intraspecific diversity as reported inidentification keys, morphological variation reportedin ecological studies, and allozyme and matingbehavior patterns. Our analysis suggests that siblingspecies may be frequent in rotifers. Monogonontrotifers seem to meet conditions for an activespeciation, wh…

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,…

A mathematical model for the phase of sexual reproduction in monogonont rotifers

Recently, the optimal sex allocation in monogonont rotifers is studied in [1], and, as a closely related question, the relative frequencies of the relevant types of mictic females. The authors focus on the evolution of the age at which young mictic females lose their fertilization susceptibility and they address the threshold age of fertilization that maximizes resting egg production. Assuming that a stationary population is achieved, with stable age distribution, they obtain their results, without knowing the stationary population. Our aim is to study this problem in the framework of the theory of nonlinear age-dependent population dynamics developed by G. F. Webb in [13], which is more ap…

Starvation tolerance of rotifers produced from parthenogenetic eggs and from diapausing eggs: a life table approach

Monogonont rotifers have to cope with environmental variation by producing diapausing stages.Cyclically, parthenogenetic rotifers produce females by (i) parthenogenetic eggs and (ii) sexuallyproduced eggs. Parthenogenetic eggs hatch shortly after ovoposition, frequently while they are carriedby their mothers. Sexual eggs go into dormancy and hatch in the sediment, in response to specificenvironmental cues. Therefore, it is expected that post-diapause and parthenogenetic offspring wouldface different environments. Moreover, resource allocation is higher in diapausing eggs than inparthenogenetic eggs. In this study, the response to starvation of females obtained from partheno-genetic eggs and …

Brachionus plicatilis tolerance to low oxygen concentrations

Tolerance to low oxygen concentrations is expected in Brachionus plicatilis, a rotifer adapted to live in saline warm waters. The population dynamics of a clone of this species, isolated from an endorreic saline lake, was studied under controlled laboratory conditions. Although their growth and metabolism is extremely reduced, B. plicatilis populations are able to maintain relatively high-density populations (a mean of 35 ind ml−1) in oxygen concentrations below 1 mgl−1, for more than one month. Major features of population growth related to oxygen are discussed.

Delayed mixis in rotifers: an adaptive response to the effects of density-dependent sex on population growth

In most cyclically parthenogenetic life cycles, sex is needed to produce resting stages. In several species of cyclically parthenogenetic rotifers, some generations of clones are not responsive to a density-dependent signal that triggers sexual female production. These unresponsive rotifers hatch from resting eggs and typically pass 8–12 generations of female parthenogenesis before becoming receptive to the mixis signal. We addressed the selection for mixis delay using a simulation model. A delay of sexual reproduction could increase population growth through parthenogenesis and thus the number of resting eggs ultimately produced. In a monomorphic population without mixis delay, we determin…

Euryhaline Brachionus strains (Rotifera) from tropical habitats: morphology and allozyme patterns

The euryhaline rotifer Brachionus is a complex of sibling species. Although many investigations have been carried out in the past, the relationships among the Spanish species, the tropical SS strains and the clusters previously described, remained unknown. In this study, allozyme data for five populations from the tropics and two from Spanish lagoons — one of them B. ibericus and the other B. rotundiformis — were combined with data from the previous studies. Cluster analysis based on genetic distance allowed the 74 strains to be divided into two major groups. One group was associated with B. plicatilis-like strains, and the other group was associated with B. rotundiformis and B. ibericus. T…

Behavioral reproductive isolation among sympatric strains of Brachionus plicatilis Müller 1786: insights into the status of this taxonomic species

We present results on cross-mating experiments using Brachionus plicatilis strains collected in three ponds of a coastal marsh (Torreblanca Marsh, Castellon, Spain). These strains were known to differ widely both in morphology and allozyme patterns from a previous study, where they were grouped into three genetically different clonal groups. Although some of the strains co-occurred in the same pond and sexual periods overlapped, no gene flow was found among them. Our first objective was to determine whether behavioral reproductive isolation was responsible for the absence of interbreeding. A second objective was to explore the relationship between sexual isolation and genetic divergence. We…

List of papers selected in bibliographic search from Ageing via perception costs of reproduction magnifies sexual selection

Understanding what factors modulate sexual selection intensity is crucial to a wide variety of evolutionary processes. Recent studies show that perception of sex pheromones can severely impact male mortality when it is not followed by mating (perception costs of reproduction). Here, we examine the idea that this may magnify sexual selection by further decreasing the fitness of males with inherently low mating success, hence increasing the opportunity for sexual selection. We use mathematical modelling to show that even modest mortality perception costs can significantly increase variability in male reproductive success under a wide range of demographic conditions. We then conduct a series o…

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…

Data from: Ageing via perception costs of reproduction magnifies sexual selection

Understanding what factors modulate sexual selection intensity is crucial to a wide variety of evolutionary processes. Recent studies show that perception of sex pheromones can severely impact male mortality when it is not followed by mating (perception costs of reproduction). Here, we examine the idea that this may magnify sexual selection by further decreasing the fitness of males with inherently low mating success, hence increasing the opportunity for sexual selection. We use mathematical modelling to show that even modest mortality perception costs can significantly increase variability in male reproductive success under a wide range of demographic conditions. We then conduct a series o…