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Despite evolutionary biology’s obsession with natural selection, few studies have evaluated multigenerational series of patterns of selection on a genome-wide scale in natural populations. Here, we report on a 10-y population-genomic survey of the microcrustaceanDaphnia pulex.The genome sequences of $>$800 isolates provide insights into patterns of selection that cannot be obtained from long-term molecular-evolution studies, including the following: the pervasiveness of near quasi-neutrality across the genome (mean net selection coefficients near zero, but with significant temporal variance about the mean, and little evidence of positive covariance of selection across time intervals); the preponderance of weak positive selection operating on minor alleles; and a genome-wide distribution of numerous small linkage islands of observable selection influencing levels of nucleotide diversity. These results suggest that interannual fluctuating selection is a major determinant of standing levels of variation in natural populations, challenge the conventional paradigm for interpreting patterns of nucleotide diversity and divergence, and motivate the need for the further development of theoretical expressions for the interpretation of population-genomic data. 

Abstract Studies of closely related species with known ecological differences provide exceptional opportunities for understanding the genetic mechanisms of evolution. In this study, we compared population-genomics data between Daphnia pulex and Daphnia pulicaria, two reproductively compatible sister species experiencing ecological speciation, the first largely confined to intermittent ponds and the second to permanent lakes in the same geographic region. Daphnia pulicaria has lower genome-wide nucleotide diversity, a smaller effective population size, a higher incidence of private alleles, and a substantially more linkage disequilibrium than D. pulex. Positively selected genes in D. pulicaria are enriched in potentially aging-related categories such as cellular homeostasis, which may explain the extended life span in D. pulicaria. We also found that opsin-related genes, which may mediate photoperiodic responses, are under different selection pressures in these two species. Genes involved in mitochondrial functions, ribosomes, and responses to environmental stimuli are found to be under positive selection in both species. Additionally, we found that the two species have similar average evolutionary rates at the DNA-sequence level, although approximately 160 genes have significantly different rates in the two lineages. Our results provide insights into the physiological traits that differ within this regionally sympatric sister-species pair that occupies unique microhabitats. 

ABSTRACT Microorganisms play a central role in sustaining soil ecosystems and agriculture, and these functions are usually associated with their complex life history. Yet, the regulation and evolution of life history have remained enigmatic and poorly understood, especially in protozoa, the third most abundant group of organisms in the soil. Here, we explore the life history of a cosmopolitan species—Colpoda steinii. Our analysis has yielded a high-quality macronuclear genome forC. steinii, with size of 155 Mbp and 37,123 protein-coding genes, as well as mean intron length of ~93 bp, longer than most other studied ciliates. Notably, we identify two possible whole-genome duplication events inC. steinii, which may account for its genome being about twice the size ofC. inflata’s, another co-existing species. We further resolve the gene expression profiles in diverse life stages ofC. steinii, which are also corroborated inC. inflata. During the resting cyst stage, genes associated with cell death and vacuole formation are upregulated, and translation-related genes are downregulated. While the translation-related genes are upregulated during the excystment of resting cysts. Reproductive cysts exhibit a significant reduction in cell adhesion. We also demonstrate that most genes expressed in specific life stages are under strong purifying selection. This study offers a deeper understanding of the life history evolution that underpins the extraordinary success and ecological functions of microorganisms in soil ecosystems.IMPORTANCEColpodaspecies, as a prominent group among the most widely distributed and abundant soil microorganisms, play a crucial role in sustaining soil ecosystems and promoting plant growth. This investigation reveals their exceptional macronuclear genomic features, including significantly large genome size, long introns, and numerous gene duplications. The gene expression profiles and the specific biological functions associated with the transitions between various life stages are also elucidated. The vast majority of genes linked to life stage transitions are subject to strong purifying selection, as inferred from multiple natural strains newly isolated and deeply sequenced. This substantiates the enduring and conservative nature ofColpoda’s life history, which has persisted throughout the extensive evolutionary history of these highly successful protozoa in soil. These findings shed light on the evolutionary dynamics of microbial eukaryotes in the ever-fluctuating soil environments. This integrative research represents a significant advancement in understanding the life histories of these understudied single-celled eukaryotes. 

Colpoda, one of the most widespread ciliated protozoa in soil, are poorly understood in regard to their genetics and evolution. Our research revealed extreme mitochondrial gene rearrangements dominated by gene loss events, potentially leading to the streamlining ofColpodamitogenomes. Surprisingly, while interspecific rearrangements abound, our population-level mitogenomic study revealed a conserved gene order within species, offering a potential new identification criterion. Phylogenomic analysis traced their lineage over 326 million years, revealing two distinct groups. Substantial genomic divergence might be associated with the lack of extended collinear blocks and relaxed purifying selection. This study systematically revealsColpodaciliate mitogenome structures and evolution, providing insights into the survival and evolution of these vital soil microorganisms. 

Abstract The field of genomics has ushered in new methods for studying molecular-genetic variation in natural populations. However, most population-genomic studies still rely on small sample sizes (typically, <100 individuals) from single time points, leaving considerable uncertainties with respect to the behavior of relatively young (and rare) alleles and, owing to the large sampling variance of measures of variation, to the specific gene targets of unusually strong selection. Genomic sequences of ∼1,700 haplotypes distributed over a 10-year period from a natural population of the microcrustacean Daphnia pulex reveal evolutionary-genomic features at a refined scale, including previously hidden information on the behavior of rare alleles predicted by recent theory. Background selection, resulting from the recurrent introduction of deleterious alleles, appears to strongly influence the dynamics of neutral alleles, inducing indirect negative selection on rare variants and positive selection on common variants. Temporally fluctuating selection increases the persistence of nonsynonymous alleles with intermediate frequencies, while reducing standing levels of variation at linked silent sites. Combined with the results from an equally large metapopulation survey of the study species, classes of genes that are under strong positive selection can now be confidently identified in this key model organism. Most notable among rapidly evolving Daphnia genes are those associated with ribosomes, mitochondrial functions, sensory systems, and lifespan determination. 

Abstract Sex determination (SD) involves mechanisms that determine whether an individual will develop into a male, female, or in rare cases, hermaphrodite. Crustaceans harbor extremely diverse SD systems, including hermaphroditism, environmental sex determination (ESD), genetic sex determination (GSD), and cytoplasmic sex determination (e.g.,Wolbachiacontrolled SD systems). Such diversity lays the groundwork for researching the evolution of SD in crustaceans, i.e., transitions among different SD systems. However, most previous research has focused on understanding the mechanism of SD within a single lineage or species, overlooking the transition across different SD systems. To help bridge this gap, we summarize the understanding of SD in various clades of crustaceans, and discuss how different SD systems might evolve from one another. Furthermore, we review the genetic basis for transitions between different SD systems (i.e.,Dmrtgenes) and propose the microcrustaceanDaphnia(clade Branchiopoda) as a model to study the transition from ESD to GSD. 

The ways in which genetic variation is distributed within and among populations is a key determinant of the evolutionary features of a species. However, most comprehensive studies of these features have been restricted to studies of subdivision in settings known to have been driven by local adaptation, leaving our understanding of the natural dispersion of allelic variation less than ideal. Here, we present a geographic population-genomic analysis of 10 populations of the freshwater microcrustacean Daphnia pulex, an emerging model system in evolutionary genomics. These populations exhibit a pattern of moderate isolation-by-distance, with an average migration rate of 0.6 individuals per generation, and average effective population sizes of ∼650,000 individuals. Most populations contain numerous private alleles, and genomic scans highlight the presence of islands of excessively high population subdivision for more common alleles. A large fraction of such islands of population divergence likely reflect historical neutral changes, including rare stochastic migration and hybridization events. The data do point to local adaptive divergence, although the precise nature of the relevant variation is diffuse and cannot be associated with particular loci, despite the very large sample sizes involved in this study. In contrast, an analysis of between-species divergence highlights positive selection operating on a large set of genes with functions nearly nonoverlapping with those involved in local adaptation, in particular ribosome structure, mitochondrial bioenergetics, light reception and response, detoxification, and gene regulation. These results set the stage for using D. pulex as a model for understanding the relationship between molecular and cellular evolution in the context of natural environments. 

By revealing the influence of recombinational activity beyond what can be achieved with controlled crosses, measures of linkage disequilibrium (LD) in natural populations provide a powerful means of defining the recombinational landscape within which genes evolve. In one of the most comprehensive studies of this sort ever performed, involving whole-genome analyses on nearly 1,000 individuals of the cyclically parthenogenetic microcrustacean Daphnia pulex, the data suggest a relatively uniform pattern of recombination across the genome. Patterns of LD are quite consistent among populations; average rates of recombination are quite similar for all chromosomes; and although some chromosomal regions have elevated recombination rates, the degree of inflation is not large, and the overall spatial pattern of recombination is close to the random expectation. Contrary to expectations for models in which crossing-over is the primary mechanism of recombination, and consistent with data for other species, the distance-dependent pattern of LD indicates excessively high levels at both short and long distances and unexpectedly low levels of decay at long distances, suggesting significant roles for factors such as nonindependent mutation, population subdivision, and recombination mechanisms unassociated with crossing over. These observations raise issues regarding the classical LD equilibrium model widely applied in population genetics to infer recombination rates across various length scales on chromosomes. 

Abstract Although obligately asexual lineages are thought to experience selective disadvantages associated with reduced efficiency of fixing beneficial mutations and purging deleterious mutations, such lineages are phylogenetically and geographically widespread. However, despite several genome-wide association studies, little is known about the genetic elements underlying the origin of obligate asexuality and how they spread. Because many obligately asexual lineages have hybrid origins, it has been suggested that asexuality is caused by the unbalanced expression of alleles from the hybridizing species. Here, we investigate this idea by identifying genes with allele-specific expression (ASE) in a Daphnia pulex population, in which obligate parthenogens (OP) and cyclical parthenogens (CP) coexist, with the OP clones having been originally derived from hybridization between CP D. pulex and its sister species, Daphnia pulicaria. OP D. pulex have significantly more ASE genes (ASEGs) than do CP D. pulex. Whole-genomic comparison of OP and CP clones revealed ∼15,000 OP-specific markers and 42 consistent ASEGs enriched in marker-defined regions. Ten of the 42 ASEGs have alleles coding for different protein sequences, suggesting functional differences between the products of the two parental alleles. At least three of these ten genes appear to be directly involved in meiosis-related processes, for example, RanBP2 can cause abnormal chromosome segregation in anaphase I, and the presence of Wee1 in immature oocytes leads to failure to enter meiosis II. These results provide a guide for future molecular resolution of the genetic basis of the transition to ameiotic parthenogenesis.