Gribble Kristin E.

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Gribble

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Kristin E.

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0000-0002-8781-9523

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The mate recognition protein gene mediates reproductive isolation and speciation in the Brachionus plicatilis cryptic species complex

(BioMed Central, 2012-08-01) Gribble, Kristin E. ; Mark Welch, David B.

Chemically mediated prezygotic barriers to reproduction likely play an important role in speciation. In facultatively sexual monogonont rotifers from the Brachionus plicatilis cryptic species complex, mate recognition of females by males is mediated by the Mate Recognition Protein (MRP), a globular glycoprotein on the surface of females, encoded by the mmr-b gene family. In this study, we sequenced mmr-b copies from 27 isolates representing 11 phylotypes of the B. plicatilis species complex, examined the mode of evolution and selection of mmr-b, and determined the relationship between mmr-b genetic distance and mate recognition among isolates. Isolates of the B. plicatilis species complex have 1–4 copies of mmr-b, each composed of 2–9 nearly identical tandem repeats. The repeats within a gene copy are generally more similar than are gene copies among phylotypes, suggesting concerted evolution. Compared to housekeeping genes from the same isolates, mmr-b has accumulated only half as many synonymous differences but twice as many non-synonymous differences. Most of the amino acid differences between repeats appear to occur on the outer face of the protein, and these often result in changes in predicted patterns of phosphorylation. However, we found no evidence of positive selection driving these differences. Isolates with the most divergent copies were unable to mate with other isolates and rarely self-crossed. Overall the degree of mate recognition was significantly correlated with the genetic distance of mmr-b. Discrimination of compatible mates in the B. plicatilis species complex is determined by proteins encoded by closely related copies of a single gene, mmr-b. While concerted evolution of the tandem repeats in mmr-b may function to maintain identity, it can also lead to the rapid spread of a mutation through all copies in the genome and thus to reproductive isolation. The mmr-b gene is evolving rapidly, and novel alleles may be maintained and increase in frequency via asexual reproduction. Our analyses indicate that mate recognition, controlled by MMR-B, may drive reproductive isolation and allow saltational sympatric speciation within the B. plicatilis cryptic species complex, and that this process may be largely neutral.
A demographic and evolutionary analysis of maternal effect senescence

(National Academy of Sciences, 2020-06-29) Hernández, Christina M. ; van Daalen, Silke F. ; Caswell, Hal ; Neubert, Michael G. ; Gribble, Kristin E.

Maternal effect senescence—a decline in offspring survival or fertility with maternal age—has been demonstrated in many taxa, including humans. Despite decades of phenotypic studies, questions remain about how maternal effect senescence impacts evolutionary fitness. To understand the influence of maternal effect senescence on population dynamics, fitness, and selection, we developed matrix population models in which individuals are jointly classified by age and maternal age. We fit these models to data from individual-based culture experiments on the aquatic invertebrate, Brachionus manjavacas (Rotifera). By comparing models with and without maternal effects, we found that maternal effect senescence significantly reduces fitness for B. manjavacas and that this decrease arises primarily through reduced fertility, particularly at maternal ages corresponding to peak reproductive output. We also used the models to estimate selection gradients, which measure the strength of selection, in both high growth rate (laboratory) and two simulated low growth rate environments. In all environments, selection gradients on survival and fertility decrease with increasing age. They also decrease with increasing maternal age for late maternal ages, implying that maternal effect senescence can evolve through the same process as in Hamilton’s theory of the evolution of age-related senescence. The models we developed are widely applicable to evaluate the fitness consequences of maternal effect senescence across species with diverse aging and fertility schedule phenotypes.
Lifespan extension by caloric restriction is determined by type and level of food reduction and by reproductive mode in Brachionus manjavacas (Rotifera)

( 2012-04-27) Gribble, Kristin E. ; Mark Welch, David B.

We measured lifespan and fecundity of three reproductive modes in a clone of the monogonont rotifer Brachionus manjavacas subjected to chronic caloric restriction (CCR) over a range of food concentrations or to intermittent fasting (IF). IF increased lifespan 50 – 70% for all three modes, while CCR increased lifespan of asexual females derived from sexually- or asexually-produced eggs, but not that of sexual females. The main effect of CR on both asexual modes was to delay death at young ages, rather than to prevent death at middle ages or to greatly extend maximum lifespan; in contrast CR in sexual females greatly increased the lifespan of a few long-lived individuals. Lifetime fecundity did not decrease with CCR, suggesting a lack of resource allocation trade-off between somatic maintenance and reproduction. Multiple outcomes for a clonal lineage indicate that different responses are established through epigenetic programming, while differences in lifespan allocations suggest that multiple genetic mechanisms mediate lifespan extension.
Rotifers as experimental tools for investigating aging

(Taylor & Francis, 2014-06-12) Snell, Terry W. ; Johnston, Rachel K. ; Gribble, Kristin E. ; Mark Welch, David B.

Comparative biogerontology has much to contribute to the study of aging. A broad range of aging rates have evolved to meet environmental challenges, and understanding these adaptations can produce valuable insights into aging. The supra Phylum Lophotrochozoa is particularly understudied and has several groups that have intriguing patterns of aging. Members of the Lophotrochozoan phylum Rotifera are particularly useful for aging studies because cohort life tables can be conducted with them easily, and biochemical and genomic tools are available for examining aging mechanisms. This paper reviews a variety of caloric restriction (CR) regimens, small molecule inhibitors, and dietary supplements that extend rotifer lifespan, as well as important interactions between CR and genotype, antioxidant supplements, and TOR and jun-N-terminal kinase (JNK) pathways, and the use of RNAi to identify key genes involved in modulating the aging response. Examples of how rapamycin and JNK inhibitor exposure keeps mortality rates low during the reproductive phase of the life cycle are presented, and the ease of conducting life table experiments to screen natural products from red algae for life extending effects is illustrated. Finally, experimental evolution to produce longer-lived rotifer individuals is demonstrated, and future directions to determine the genetic basis of aging are discussed.
The contributions of maternal age heterogeneity to variance in lifetime reproductive output

(The University of Chicago Press, 2022-03-28) van Daalen, Silke F. ; Hernández, Christina M. ; Caswell, Hal ; Neubert, Michael G. ; Gribble, Kristin E.

Variance among individuals in fitness components reflects both genuine heterogeneity between individuals and stochasticity in events experienced along the life cycle. Maternal age represents a form of heterogeneity that affects both the mean and the variance of lifetime reproductive output (LRO). Here, we quantify the relative contribution of maternal age heterogeneity to the variance in LRO using individual-level laboratory data on the rotifer Brachionus manjavacas to parameterize a multistate age × maternal age matrix model. In B. manjavacas, advanced maternal age has large negative effects on offspring survival and fertility. We used multistate Markov chains with rewards to quantify the contributions to variance in LRO of heterogeneity and of the stochasticity inherent in the outcomes of probabilistic transitions and reproductive events. Under laboratory conditions, maternal age heterogeneity contributes 26% of the variance in LRO. The contribution changes when mortality and fertility are reduced to mimic more ecologically relevant environments. Over the parameter space where populations are near stationarity, maternal age heterogeneity contributes an average of 3% of the variance. Thus, the contributions of maternal age heterogeneity and individual stochasticity can be expected to depend strongly on environmental conditions; over most of the parameter space, the variance in LRO is dominated by stochasticity.
Genome-wide transcriptomics of aging in the rotifer Brachionus manjavacas, an emerging model system

(BioMed Central, 2017-03-01) Gribble, Kristin E. ; Mark Welch, David B.

Understanding gene expression changes over lifespan in diverse animal species will lead to insights to conserved processes in the biology of aging and allow development of interventions to improve health. Rotifers are small aquatic invertebrates that have been used in aging studies for nearly 100 years and are now re-emerging as a modern model system. To provide a baseline to evaluate genetic responses to interventions that change health throughout lifespan and a framework for new hypotheses about the molecular genetic mechanisms of aging, we examined the transcriptome of an asexual female lineage of the rotifer Brachionus manjavacas at five life stages: eggs, neonates, and early-, late-, and post-reproductive adults. There are widespread shifts in gene expression over the lifespan of B. manjavacas; the largest change occurs between neonates and early reproductive adults and is characterized by down-regulation of developmental genes and up-regulation of genes involved in reproduction. The expression profile of post-reproductive adults was distinct from that of other life stages. While few genes were significantly differentially expressed in the late- to post-reproductive transition, gene set enrichment analysis revealed multiple down-regulated pathways in metabolism, maintenance and repair, and proteostasis, united by genes involved in mitochondrial function and oxidative phosphorylation. This study provides the first examination of changes in gene expression over lifespan in rotifers. We detected differential expression of many genes with human orthologs that are absent in Drosophila and C. elegans, highlighting the potential of the rotifer model in aging studies. Our findings suggest that small but coordinated changes in expression of many genes in pathways that integrate diverse functions drive the aging process. The observation of simultaneous declines in expression of genes in multiple pathways may have consequences for health and longevity not detected by single- or multi-gene knockdown in otherwise healthy animals. Investigation of subtle but genome-wide change in these pathways during aging is an important area for future study.
The ecology, life history, and phylogeny of the marine thecate heterotrophic dinoflagellates Protoperidinium and Diplopsalidaceae (Dinophyceae)

(Massachusetts Institute of Technology and Woods Hole Oceanographic Institution, 2006-09) Gribble, Kristin E.

Marine thecate heterotrophic dinoflagellates likely play an important role in the consumption of primary productivity and in the trophic structure of the plankton, yet we know little about these species. This thesis expanded our understanding of the autecology and evolutionary history of the Protoperidinium and diplopsalids. The distributions of Protoperidinium species off the southwestern coast of Ireland were influenced by physical oceanographic conditions coupled with the availability of preferred prey. The distributions of individual Protoperidinium species varied widely from the distribution of total Protoperidinium, indicating differences in ecologies among species. Certain species of Protoperidinium co-occurred with known preferred phytoplankton prey species. Concentrations of other Protoperidinium species were not related to those of any particular phytoplankton species, indicating that these Protoperidinium may rely on phytoplankton or other food sources beyond those already known, may not be species specific selective feeders, or may have become uncoupled from their preferred prey. The description of the sexual and asexual life history of Protoperidinium steidingerae provided the first account of the life history of any Protoperidinium species. Asexual division occurred by eleutheroschisis within a temporary, immotile cyst, yielding two daughter cells. Daughter cells were initially round and half to two-thirds the size of parent cells, then rapidly increased in size, forming horns before separating. Sexual reproduction was constitutive in clonal cultures, indicating that the species may be homothallic. Fusing gametes were isogamous, and resulted in a planozygote with two longitudinal flagella. Hypnozygotes had a mandatory dormancy period of ca. 70 days. Germination resulted in planomeiocytes with two longitudinal flagella. Nuclear cyclosis may occur in the planomeiocyte stage. A high level of morphological diversity among life history stages of P. steidingerae has led to mis-classification and taxonomic inaccuracy of Protoperidinium species identified from field samples. The large subunit ribosomal DNA (LSU rDNA) molecular phylogeny of the heterotrophic dinoflagellates revealed that the genus Protoperidinium appeared to be recently diverged within the dinoflagellates. In maximum parsimony and neighbor joining analysis, Protoperidinium formed a monophyletic group, evolving from diplopsalid dinoflagellates. In maximum likelihood and Bayesian analyses, however, Protoperidinium was polyphyletic, as the lenticular, diplopsalid heterotroph, Diplopsalis lenticula Bergh, was inserted within the Protoperidinium clade basal to Protoperidinium excentricum (Paulsen) Balech, and Preperidinium meunieri (Pavillard) Elbrächter fell within a separate clade as a sister to the Oceanica section and Protoperidinium steidingerae Balech. In all analyses, the Protoperidinium were divided into two major clades, with members in the Oceanica group and subgenus Testeria in one clade, and the Excentrica, Conica, Pellucida, Pyriforme, and Divergens sections in another clade. The LSU rDNA molecular phylogeny supported the historical morphologically determined sections, but not a simple morphology-based model of evolution based on thecal plate shape. LSU rDNA gene sequences are frequently used to infer the phylogeny of organisms. The many copies of the LSU rDNA found in the genome are thought to be kept homogenous by concerted evolution. In Protoperidinium species, however, there was high intragenomic diversity in the D1-D6 region of the LSU rDNA. For each species, the clone library was usually comprised of one highly represented copy and many unique sequences. Sequence differences were primarily characterized by single base pair substitutions, single base pair insertion/deletions (indels), and/or large indels. Phylogenetic analysis of all clones gave strong support for monophyly of the polymorphic copies of each species, and recovered the same species tree as an analysis using just one sequence per species. Analysis of LSU rDNA gene expression in three species by RT-PCR indicated that copies with fewer substitutions and fewer and smaller indels are expressed, and that 50% or more of the copies are pseudogenes. High intraspecific and intraindividual LSU rDNA sequence variability could lead to inaccurate species phylogenies and over-estimation of species diversity in environmental sequencing studies. This thesis has explored the ecology, life history, molecular phylogeny, and intraspecific DNA sequence variability of marine thecate heterotrohic dinoflagellates using a wide range of methodologies, including field sampling, culturing, microscopy, morphological analyses, histological staining, and molecular biology. The work here has broadened our understanding of the Protoperidinium and diplopsalids, providing new insights into the ecological and evolutionary relationships of these heterotrophs with other plankton species.
SAG-RAD: a method for single-cell population genomics of unicellular eukaryotes

(Oxford University Press, 2023-04-20) Gollnisch, Raphael ; Wallenius, Joel ; Gribble, Kristin E. ; Ahrén, Dag ; Rengefors, Karin

Sequencing of reduced representation libraries enables genotyping of many individuals for population genomic studies. However, high amounts of DNA are required, and the method cannot be applied directly on single cells, preventing its use on most microbes. We developed and implemented the analysis of single amplified genomes followed by restriction-site-associated DNA sequencing to bypass labor-intensive culturing and to avoid culturing bias in population genomic studies of unicellular eukaryotes. This method thus opens the way for addressing important questions about the genetic diversity, gene flow, adaptation, dispersal, and biogeography of hitherto unexplored species.
Maternal caloric restriction partially rescues the deleterious effects of advanced maternal age on offspring

(Anatomical Society and John Wiley & Sons, 2014-03-24) Gribble, Kristin E. ; Jarvis, George ; Bock, Martha ; Mark Welch, David B.

While many studies have focused on the detrimental effects of advanced maternal age and harmful prenatal environments on progeny, little is known about the role of beneficial non-Mendelian maternal inheritance on aging. Here, we report the effects of maternal age and maternal caloric restriction (CR) on the life span and health span of offspring for a clonal culture of the monogonont rotifer Brachionus manjavacas. Mothers on regimens of chronic CR (CCR) or intermittent fasting (IF) had increased life span compared with mothers fed ad libitum (AL). With increasing maternal age, life span and fecundity of female offspring of AL-fed mothers decreased significantly and life span of male offspring was unchanged, whereas body size of both male and female offspring increased. Maternal CR partially rescued these effects, increasing the mean life span of AL-fed female offspring but not male offspring and increasing the fecundity of AL-fed female offspring compared with offspring of mothers of the same age. Both maternal CR regimens decreased male offspring body size, but only maternal IF decreased body size of female offspring, whereas maternal CCR caused a slight increase. Understanding the genetic and biochemical basis of these different maternal effects on aging may guide effective interventions to improve health span and life span.

Gribble Kristin E.

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