Spatial versus spatio-temporal approaches for studying metacommunities: a multi-taxon analysis in Mediterranean and tropical temporary ponds.

Prior research on metacommunities has largely focused on snapshot surveys, often overlooking temporal dynamics. In this study, our aim was to compare the insights obtained from metacommunity analyses based on a spatial approach repeated over time, with a spatio-temporal approach that consolidates all data into a single model. We empirically assessed the influence of temporal variation in the environment and spatial connectivity on the structure of metacommunities in tropical and Mediterranean temporary ponds. Employing a standardized methodology across both regions, we surveyed multiple freshwater taxa in three time periods within the same hydrological year from multiple temporary ponds in each region. To evaluate how environmental, spatial and temporal influences vary between the two approaches, we used nonlinear variation partitioning analyses based on generalized additive models. Overall, this study underscores the importance of adopting spatio-temporal analytics to better understand the processes shaping metacommunities. While the spatial approach suggested that environmental factors had a greater influence, our spatio-temporal analysis revealed that spatial connectivity was the primary driver influencing metacommunity structure in both regions. Temporal effects were equally important as environmental effects, suggesting a significant role of ecological succession in metacommunity structure.

Inconsistent response of taxonomic groups to space and environment in mediterranean and tropical pond metacommunities.

The metacommunity concept provides a theoretical framework that aims at explaining organism distributions by a combination of environmental filtering, dispersal, and drift. However, few works have attempted a multitaxon approach and even fewer have compared two distant biogeographical regions using the same methodology. We tested the expectation that temperate (mediterranean-climate) pond metacommunities would be more influenced by environmental and spatial processes than tropical ones, because of stronger environmental gradients and a greater isolation of waterbodies. However, the pattern should be different among groups of organisms depending on their dispersal abilities. We surveyed 30 tropical and 32 mediterranean temporary ponds from Costa Rica and Spain, respectively, and obtained data on 49 environmental variables. We characterized the biological communities of bacteria and archaea (from the water column and the sediments), phytoplankton, zooplankton, benthic invertebrates, amphibians and birds, and estimated the relative role of space and environment on metacommunity organization for each group and region, by means of variation partitioning using generalized additive models. Purely environmental effects were important in both tropical and mediterranean ponds, but stronger in the latter, probably due to their larger limnological heterogeneity. Spatially correlated environment and pure spatial effects were greater in the tropics, related to higher climatic heterogeneity and dispersal processes (e.g., restriction, surplus) acting at different scales. The variability between taxonomic groups in the contribution of spatial and environmental factors to metacommunity variation was very wide, but higher in active, compared with passive, dispersers. Higher environmental effects were observed in mediterranean passive dispersers, and higher spatial effects in tropical passive dispersers. The unexplained variation was larger in the tropical setting, suggesting a higher role for stochastic processes, unmeasured environmental factors, or biotic interactions in the tropics, although this difference affected some actively dispersing groups (insects and birds) more than passive dispersers. These results, despite our limitations in comparing only two regions, provide support, for a wide variety of aquatic organisms, for the classic view of stronger abiotic niche constraints in temperate areas compared with the tropics. The heterogeneous response of taxonomic groups between regions also points to a stronger influence of regional context than organism adaptations on metacommunity organization.

Gene expression in diapausing rotifer eggs in response to divergent environmental predictability regimes.

In 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 combinations of two contrasting selective regimes of environmental fluctuation (predictable vs unpredictable) and two different diapause conditions (passing or not passing through forced diapause). The results showed that the selective regime was more important than the diapause condition in driving differences in the transcriptome profile. Most of the differentially expressed genes were upregulated in the predictable regime and mostly associated with molecular functions involved in embryo morphological development and hatching readiness. This was in concordance with observations of earlier, higher, and more synchronous hatching in diapausing eggs produced under the predictable regime.

Physical models of infant mortality: implications for defects in biological systems.

Reliability engineering concerned with failure of technical inanimate systems usually uses the vocabulary and notions of human mortality, e.g., infant mortality vs. senescence mortality. Yet, few data are available to support such a parallel description. Here, we focus on early-stage (infant) mortality for two inanimate systems, incandescent light bulbs and soap films, and show the parallel description is clearly valid. Theoretical considerations of the thermo-electrical properties of electrical conductors allow us to link bulb failure to inherent mechanical defects. We then demonstrate the converse, that is, knowing the failure rate for an ensemble of light bulbs, it is possible to deduce the distribution of defects in wire thickness in the ensemble. Using measurements of lifetimes for soap films, we show how this methodology links failure rate to geometry of the system; in the case presented, this is the length of the tube containing the films. In a similar manner, for a third example, the time-dependent death rate due to congenital aortic valve stenosis is related to the distribution of degrees of severity of this condition, as a function of time. The results not only validate clearly the parallel description noted above, but also point firmly to application of the methodology to humans, with the consequent ability to gain more insight into the role of abnormalities in infant mortality.

Magnitude and significance of the peak of early embryonic mortality.

Embryonic development is of great importance because it determines congenital anomalies and influences their severity. However, little is known about the actual probabilities of success or failure and about the nature of early embryonic defects. Here, we propose that the analysis of embryonic mortality as a function of post-fertilization time provides a simple way to identify major defects. By reviewing the literature, we show that even small initial defects, e.g., spatial cellular asymmetries or irregularities in the timing of development, carry with them lethal effects in subsequent stages of embryogenesis. Although initially motivated by human study, in this contribution, we review the few embryonic mortality data available for farm animals and highlight zebrafish as a particularly suited organism for such a kind of study because embryogenesis can be followed from its very beginning and observed easily thanks to eggshell transparency. In line with the few other farm animals for which data are available, we provide empirical evidence that embryonic mortality in zebrafish has a prominent peak shortly after fertilization. Indeed, we show how subsequent mortality rates decay according to a power law, supporting the role of the early embryonic mortality peak as a screening process rapidly removing defective embryos.

Ecological genomics of adaptation to unpredictability in experimental rotifer populations.

Elucidating 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 using genotyping by sequencing (GBS). Additionally, we used GBS data from the 270 field clones from which the laboratory populations were established. This GBS dataset was used to identify candidate SNPs under selection. A total of 76 SNPs showed divergent selection, three of which are candidates for being under selection in the particular unpredictable fluctuation pattern studied. Most of the remaining SNPs showed strong signals of adaptation to laboratory conditions. Furthermore, a genotype-phenotype association approach revealed five SNPs associated with two key life-history traits in the adaptation to unpredictability. Our results contribute to elucidating the genomic basis for adaptation to unpredictable environments and lay the groundwork for future evolution studies in rotifers.

Facing Adversity: Dormant Embryos in Rotifers.

An in-depth look at the basic aspects of dormancy in cyclic parthenogenetic organisms is now possible thanks to research efforts conducted over the past two decades with rotifer dormant embryos. In this review, we assemble and compose the current knowledge on four central themes: (1) distribution of dormancy in animals, with an overview on the phylogenetic distribution of embryo dormancy in metazoans, and (2) physiological and cellular processes involved in dormancy, with a strong emphasis on the dormant embryos of cyclically parthenogenetic monogonont rotifers; and discussions of (3) the selective pressures and (4) the evolutionary and population implications of dormancy in these animals. Dormancy in metazoans is a widespread phenomenon with taxon-specific features, and rotifers are among the animals in which dormancy is an intrinsic feature of their life cycle. Our review shows that embryo dormancy in rotifers shares common functional pathways with other taxa at the molecular and cellular level, despite the independent evolution of dormancy across phyla. These pathways include the arrest of similar metabolic routes and the usage of common metabolites for the stabilization of cellular structures and to confer stress resistance. We conclude that specific features of recurrent harsh environmental conditions are a powerful selective pressure for the fine-tuning of dormancy patterns in rotifers. We hypothesize that similar mechanisms at the organism level will lead to similar adaptive consequences at the population level across taxa, among which the formation of egg banks, the coexistence of species, and the possibility of differentiation among populations and local adaptation stand out. Our review shows how studies of rotifers have contributed to improved knowledge of all of these aspects.

Genomic signatures of local adaptation to the degree of environmental predictability in rotifers.

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.

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.