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1. Adaptive Divergence of Meiotic Recombination Rate in Ecological Speciation

   https://doi.org/10.1093/gbe/evaa182  

   Neupane, Swatantra ; Xu, Sen ( October 2020 , Genome Biology and Evolution)

   Baer, Charles (Ed.)

   Abstract Theories predict that directional selection during adaptation to a novel habitat results in elevated meiotic recombination rate. Yet the lack of population-level recombination rate data leaves this hypothesis untested in natural populations. Here, we examine the population-level recombination rate variation in two incipient ecological species, the microcrustacean Daphnia pulex (an ephemeral-pond species) and Daphnia pulicaria (a permanent-lake species). The divergence of D. pulicaria from D. pulex involved habitat shifts from pond to lake habitats as well as strong local adaptation due to directional selection. Using a novel single-sperm genotyping approach, we estimated the male-specific recombination rate of two linkage groups in multiple populations of each species in common garden experiments and identified a significantly elevated recombination rate in D. pulicaria. Most importantly, population genetic analyses show that the divergence in recombination rate between these two species is most likely due to divergent selection in distinct ecological habitats rather than neutral evolution. 

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2. The roles of recombination and selection in shaping genomic divergence in an incipient ecological species complex

   https://doi.org/10.1111/mec.16383  

   Wersebe, Matthew J. ; Sherman, Ryan E. ; Jeyasingh, Punidan D. ; Weider, Lawrence J. ( February 2022 , Molecular Ecology)

   Speciation genomic studies have revealed that genomes of diverging lineages are shaped jointly by the actions of gene flow and selection. These evolutionary forces acting in concert with processes such as recombination and genome features such as gene density shape a mosaic landscape of divergence. We investigated the roles of recombination and gene density in shaping the patterns of differentiation and divergence between the cyclically parthenogenetic ecological sister‐taxa,Daphnia pulicariaandDaphnia pulex. First, we assembled a phased chromosome‐scale genome assembly using trio‐binning forD.pulicariaand constructed a genetic map using an F2‐intercross panel to understand sex‐specific recombination rate heterogeneity. Finally, we used a ddRADseq data set with broad geographic sampling ofD.pulicaria,D.pulex, and their hybrids to understand the patterns of genome‐scale divergence and demographic parameters. Our study provides the first sex‐specific estimates of recombination rates for a cyclical parthenogen, and unlike other eukaryotic species, we observed male‐biased heterochiasmy inD.pulicaria, which may be related to this somewhat unique breeding mode. Additionally, regions of high gene density and recombination are generally more divergent than regions of suppressed recombination. Outlier analysis indicated that divergent genomic regions are probably driven by selection onD.pulicaria, the derived lineage colonizing a novel lake habitat. Together, our study supports a scenario of selection acting on genes related to local adaptation shaping genome‐wide patterns of differentiation despite high local recombination rates in this species complex. Finally, we discuss the limitations of our data in light of demographic uncertainty.

    

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3. Genome-Wide Allele-Specific Expression in Obligately Asexual Daphnia pulex and the Implications for the Genetic Basis of Asexuality

   https://doi.org/10.1093/gbe/evab243  

   Ye, Zhiqiang ; Jiang, Xiaoqian ; Pfrender, Michael E ; Lynch, Michael ( November 2021 , Genome Biology and Evolution)

   Betancourt, Andrea (Ed.)

   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. 

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4. Genetic diversity, heteroplasmy, and recombination in mitochondrial genomes in Daphnia pulex, Daphnia pulicaria, and Daphnia obtusa.

   https://doi.org/10.1093/molbev/msac059  

   Ye, Zhiqiang ; Zhao, Chaoxian ; Raborn, R. Taylor ; Lin, Man ; Wei, Wen ; Hao, Yue ; Lynch, Michael ; Crandall, Keith ( January 2022 , Molecular biology and evolution)

   Genetic variants of mitochondrial DNA at the individual (heteroplasmy) and population (polymorphism) levels provide insight into their roles in multiple cellular and evolutionary processes. However, owing to the paucity of genome-wide data at the within-individual and population levels, the broad patterns of these two forms of variation remain poorly understood. Here, we analyze 1,804 complete mitochondrial genome sequences from Daphnia pulex, Daphnia pulicaria, and Daphnia obtusa. Extensive heteroplasmy is observed in D. obtusa, where the high level of intraclonal divergence must have resulted from a biparental-inheritance event, and recombination in the mitochondrial genome is apparent, although perhaps not widespread. Global samples of D. pulex reveal remarkably low mitochondrial effective population sizes, <3% of those for the nuclear genome. In addition, levels of population diversity in mitochondrial and nuclear genomes are uncorrelated across populations, suggesting an idiosyncratic evolutionary history of mitochondria in D. pulex. These population-genetic features appear to be a consequence of background selection associated with highly deleterious mutations arising in the strongly linked mitochondrial genome, which is consistent with polymorphism and divergence data suggesting a predominance of strong purifying selection. Nonetheless, the fixation of mildly deleterious mutations in the mitochondrial genome also appears to be driving positive selection on genes encoded in the nuclear genome whose products are deployed in the mitochondrion. 

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5. Population Genomics of Daphnia pulex

   https://doi.org/10.1534/genetics.116.190611  

   Lynch, Michael ; Gutenkunst, Ryan ; Ackerman, Matthew ; Spitze, Ken ; Ye, Zhiqiang ; Maruki, Takahiro ; Jia, Zhiyuan ( May 2017 , Genetics)

   null (Ed.)

   Abstract Using data from 83 isolates from a single population, the population genomics of the microcrustacean Daphnia pulex are described and compared to current knowledge for the only other well-studied invertebrate, Drosophila melanogaster. These two species are quite similar with respect to effective population sizes and mutation rates, although some features of recombination appear to be different, with linkage disequilibrium being elevated at short (<100 bp) distances in D. melanogaster and at long distances in D. pulex. The study population adheres closely to the expectations under Hardy–Weinberg equilibrium, and reflects a past population history of no more than a twofold range of variation in effective population size. Fourfold redundant silent sites and a restricted region of intronic sites appear to evolve in a nearly neutral fashion, providing a powerful tool for population genetic analyses. Amino acid replacement sites are predominantly under strong purifying selection, as are a large fraction of sites in UTRs and intergenic regions, but the majority of SNPs at such sites that rise to frequencies >0.05 appear to evolve in a nearly neutral fashion. All forms of genomic sites (including replacement sites within codons, and intergenic and UTR regions) appear to be experiencing an ∼2× higher level of selection scaled to the power of drift in D. melanogaster, but this may in part be a consequence of recent demographic changes. These results establish D. pulex as an excellent system for future work on the evolutionary genomics of natural populations. 

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