Eduardo M. García-Roger

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 clones of a Brachionus plicatilis rotifer population in a temporary Mediterranean pond during the period the species occurred in plankton. Clonal isolates displayed high heritable variation in their propensity for sex. Moreover, the frequency of clones with low propensity for sex increased during the growing season, which supports the hypothesized short‐term selection for low investment in sex within a growing season. These results demonstrate (1) the inherent instability of the cyclical parthenogenetic life cycle, (2) the cost of sexual reproduction in cyclical parthenogens where sex produces diapausing eggs and (3) the role of the association between sexual reproduction and diapause in maintaining sex in these cyclical parthenogens.

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 measured in four temperature × salinity combinations in common‐garden experiments. Population differentiation for neutral genetic markers – 11 microsatellite loci – was very high (FST = 0.482). Differentiation in life‐history traits was higher in traits related to sexual reproduction than in those related to asexual reproduction. QST values for diapausing egg production (a trait related to sexual reproduction) were higher than their corresponding FST in some pairs of populations. Our results indicate the importance of divergent natural selection in these populations and suggest local adaptation to the unpredictability of B. plicatilis habitats.

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 found, however, individuals from each species showed extensive overlap. Our morphometric data provide additional evidence for the species status of B. plicatilis s.s. and B. ‘Manjavacas’. Since these are ancient species, our results support that a morphological stasis occurs in these taxa. We identified COI restriction sites for PvuII and KpnI which are diagnostic for B. ‘Manjavacas’ and B. plicatilis s.s., respectively. We conclude that morphometry is not useful in classifying the two species. At present, this can only be done reliably using molecular methods.

Local adaptation in rotifer populations

The adaptation of organisms to their environment has been a subject of study for a long time. One method to study adaptations in populations involves comparing contemporary populations of the same species under different selective regimes, in what is known as a ‘local adaptation’ study. A previous study of the cyclically parthenogenetic rotifer Brachionus plicatilis found high heritabilities for some life-history traits. Some of these life-history traits significantly differed among six populations from Eastern Spain and data suggested some traits to have higher evolutionary rates than neutral genetic markers. Here, by studying the same B. plicatilis populations, we examine the variation and possible local adaptation of their main life-history traits, closely related to fitness, in relation to habitat salinity and temperature. These environmental factors have been shown to play a key role in the ecological differentiation among co-generic species of B. plicatilis. The results obtained in this study show that: (1) the seasonality of rotifer populations from Eastern Spain has profoundly influenced sexual reproduction strategies; (2) salinity is probably a key factor in the ecological specialization of some populations; and (3) rotifer populations harbour high variability in their fitness components.

Assessing rotifer diapausing egg bank diversity and abundance in brackish temporary environments : an ex situ sediment incubation approach

The hatching of diapausing eggs from sediment samples of ponds and lakes is a fast, easy, and economical technique proven useful for the assessment of diversity and abundance of zooplankton in permanent habitats. Here, we extend and optimize this approach for temporary brackish ponds which may experience great within-year variation in salinity conditions. We studied the species and numbers of rotifers emerging from the sediments of several brackish ponds and saline lakes from Eastern Spain incubated at the full range of salinity conditions observed at the study sites. On average, 82 % of the total observed species in weekly sampling for one year were detected in a single sample of both the sediments and water column. No statistical difference was found between both methods. However, some rotifer species were only observed in the water column samples, but not in sediment hatchlings, and vice versa. We concluded that both methods are not exhaustive by themselves but are complementary. Salinity affected the estimation of both rotifer richness and the density of individuals of each rotifer species that emerged from the incubated sediments. Differences in the density of emerging animals were also found among sites and among combinations of sites and salinities. The latter result indicates that in order to obtain an estimate of the emergence rate for each rotifer species present at a site, it is necessary to incubate sediments at salinity conditions close to their local values.

Being first increases the probability of long diapause in rotifer resting eggs

Monogonont rotifers typically undergo diapause to overpass adverse periods and often show within-population variation in diapause duration. Whether such variation corresponds to phenotypic plasticity, genetic polymorphism, or a bet-hedging strategy to cope with environmental unpredictability still remains unanswered. While bet hedging in diapause duration is often invoked in the rotifer literature, empirical evidence is scant and the description of a proximate mechanism responsible of the within-genotype variation required for bet hedging is still pending. We experimentally explored the role of maternal effects as responsible for the variability observed in the timing of resting egg hatching. By tracking the offspring of controlled crosses in clonal lineages of Brachionus plicatilis, we tested for differences in resting egg diapause duration due to (1) clone effect (controlling for genetic variability), (2) mother effect within clones, and (3) mother age and laying order (as candidate proximate factors explaining variability). We found a significant effect of laying order: the first eggs produced exhibited longer diapauses than eggs produced later. Finally, we critically discussed the idea that if rotifer mothers within a clone cannot anticipate the environment their offspring will experience, then they may produce resting eggs that vary in their timing of hatching via this maternal effect.

An alien ectosymbiotic branchiobdellidan (Annelida: Clitellata) adopting exotic crayfish: a biological co-invasion with unpredictable consequences

Abstract Invasive alien species present a global threat to biodiversity, particularly where pathogens and symbionts are involved. Branchiobdellidans are clitellate annelids with an obligate ectosymbiotic association primarily on astacoidean crayfish. There are several examples of branchiobdellidan species adopting a geographically exotic host where endemic and exotic crayfishes cohabit the same water body. The first records of a western North American branchiobdellidan, Xironogiton victoriensis, adopting the eastern North American crayfish, Procambarus clarkii, in 2 river basins in Spain provide further evidence of the ectosymbionts’ tolerance to adopt an exotic host. Given worldwide translocations of these and other commercial crayfish species, limnologists and agency managers need to be alert for further introductions of X. victoriensis and other branchiobdellidans. Impacts of these exotic ectosymbionts on habitat and biota at a new location are unknown, as are their consequences on native biodiversity.

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 empirical evidence for bet hedging in the scarce studies available, and we call for the need of research at different levels of biological complexity to fully understand bet hedging in rotifer diapause.

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 the level of environmental unpredictability is directly related to the propensity for sex and inversely related to the hatching fraction of diapausing eggs. We found significant levels of genetic variation within populations for both traits. Interestingly, a positive correlation between pond unpredictability—quantified in a previous study from satellite imagery—and the propensity for sex was found. This correlation suggests a conservative, bet-hedging strategy that provides protection against unexpectedly short growing seasons. By contrast, the hatching fraction of diapausing eggs was not related to the level of environmental predictability. Our results highlight the ability of rotifer populations to locally adapt to time-varying environments, providing an evolutionarily relevant step forward in relating life-history traits to a quantitative measure of environmental unpredictability.

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 included 20 Mediterranean saline ponds and lakes, and the focal variable was the water-surface area. This study first aimed to produce a method for accurately estimating the water-surface area from satellite images. Saline ponds can develop salt-crusted areas that make it difficult to distinguish between soil and water. This challenge was addressed using a novel pipeline that combines band ratio water indices and the short near-infrared band as a salt filter. The study then extracted the predictable and unpredictable components of variation in the water-surface area. Two different approaches, each showing variations in the parameters, were used to obtain the stochastic variation around a regular pattern with the objective of dissecting the effect of assumptions on predictability estimations. The first approach, which is based on Colwell’s predictability metrics, transforms the focal variable into a nominal one. The resulting discrete categories define the relevant variations in the water-surface area. In the second approach, we introduced General Additive Model (GAM) fitting as a new metric for quantifying predictability. Both approaches produced a wide range of predictability for the studied ponds. Some model assumptions–which are considered very different a priori–had minor effects, whereas others produced predictability estimations that showed some degree of divergence. We hypothesize that these diverging estimations of predictability reflect the effect of fluctuations on different types of organisms. The fluctuation analysis described in this manuscript is applicable to a wide variety of systems, including both aquatic and non-aquatic systems, and will be valuable for quantifying and characterizing predictability, which is essential within the expected global increase in the unpredictability of environmental fluctuations. We advocate that a priori information for organisms of interest should be used to select the most suitable metrics for estimating predictability, and we provide some guidelines for this approach.