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 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.

Environmental 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, phenotypic and genomic data for the same populations– to understand the genomic basis of this diverging adaptation. Firstly, a novel draft genome for B. plicatilis was assembled. Then, genome-wide polymorphisms were studied using genotyping by sequencing on 270 clones from nine populations in eastern Spain. As a result, 4,543 high-quality SNPs were identified and genotyped. More than 90 SNPs were found to be putatively under selection with signatures of diversifying and balancing selection. Over 140 SNPs were correlated with environmental or phenotypic variables revealing signatures of local adaptation, including environmental predictability. Putative functions were associated to most of these SNPs, since they were located within annotated genes. Our results reveal associations between genomic variation and the degree of environmental predictability, providing genomic evidence of adaptation to local conditions in natural rotifer populations.

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.

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 higher temperature, as compared to body size at lower temperature. The pattern was consistent for the size of both mature females and eggs; rotifers kept at high temperature evolved to be on average 14% (after 2 weeks) and 3% (after 3 weeks) smaller than the ones kept at low temperature (10 and 5% in the case of eggs, respectively). We therefore found that B. plicatilis is genetically programmed to adjust its body size-toenvironmental temperature.