scholarly journals Genetic variation for mitochondrial function in the New Zealand freshwater snail Potamopyrgus antipodarum

2016 ◽  
Author(s):  
Joel Sharbrough ◽  
Jennifer L. Cruise ◽  
Megan Beetch ◽  
Nicole M. Enright ◽  
Maurine Neiman

ABSTRACTThe proteins responsible for mitochondrial function are encoded by two different genomes with distinct inheritance regimes, rendering rigorous inference of genotype-phenotype connections intractable for all but a few model systems. Asexual organisms provide a powerful means for addressing these challenges because offspring produced without recombination inherit both nuclear and mitochondrial genomes from a single parent. As such, these offspring inherit mitonuclear genotypes that are identical to the mitonuclear genotypes of their parents and siblings and different from those of other asexual lineages. Here, we compared mitochondrial function across distinct asexual lineages of Potamopyrgus antipodarum, a New Zealand freshwater snail model for understanding the evolutionary consequences of asexuality. Our analyses revealed substantial phenotypic variation across asexual lineages at three levels of biological organization: mitogenomic, organellar, and organismal. These data demonstrate that different asexual lineages have different mitochondrial function phenotypes and that there exists heritable variation (that is, the raw material for evolution) for mitochondrial function in P. antipodarum. The discovery of this variation combined with the methods developed here sets the stage to use P. antipodarum to study central evolutionary questions involving mitochondrial function, including whether mitochondrial mutation accumulation influences the maintenance of sexual reproduction in natural populations.

2017 ◽  
Vol 108 (7) ◽  
pp. 759-768 ◽  
Author(s):  
Joel Sharbrough ◽  
Jennifer L Cruise ◽  
Megan Beetch ◽  
Nicole M Enright ◽  
Maurine Neiman

Behaviour ◽  
2000 ◽  
Vol 137 (9) ◽  
pp. 1141-1151 ◽  
Author(s):  
◽  

AbstractParasites often influence the behavior of their hosts in ways that increase the probability of transmission of the parasite. The digenetic trematode Microphallus sp. has been demonstrated to alter the behavior of the New Zealand freshwater snail Potamopyrgus antipodarum in a way that increases the probability that infected snails will be eaten by the final host (waterfowl). Infected snails are found foraging on top of rocks more often in the early morning when waterfowl are feeding and less often in the afternoon when unsuitable hosts (fish) are feeding. The mechanism(s) that the parasite utilizes to produce this behavioral change is not known. The present study investigated three possible behaviors (phototaxis, geotaxis, and photokinesis) that the parasite could alter that may account for the behavioral change seen in the field. Infected and uninfected snails were assessed in terms of their orientation to light (phototaxis), orientation to gravity (geotaxis), and movement in response to light (photokinesis). There was no evidence of phototactic behaviors in either infected or uninfected snails. However, uninfected snails were found to positively orient towards gravity, while infected snails did not. Also, both infected and uninfected snails were found to be positively photokinetic (they move faster in the light than in the dark), but Microphallus infected snails were found to move more slowly than uninfected snails. The differences found between infected and uninfected snails may be part of the manipulative effort of the parasite, but by themselves the differences are not sufficient to explain the patterns observed in the field.


2017 ◽  
Author(s):  
Emma S. Greimann ◽  
Samuel F. Ward ◽  
James D. Woodell ◽  
Samantha Hennessey ◽  
Michael R. Kline ◽  
...  

ABSTRACTMitochondrial function is critical for energy homeostasis and should shape how genetic variation in metabolism is transmitted through levels of biological organization to generate stability in organismal performance. Mitochondrial function is encoded by genes in two distinct and separately inherited genomes – the mitochondrial genome and the nuclear genome – and selection is expected to maintain functional mito-nuclear interactions. Nevertheless, high levels of polymorphism in genes involved in these mito-nuclear interactions and variation for mitochondrial function are nevertheless frequently observed, demanding an explanation for how and why variability in such a fundamental trait is maintained. Potamopyrgus antipodarum is a New Zealand freshwater snail with coexisting sexual and asexual individuals and, accordingly, contrasting systems of separate vs. co-inheritance of nuclear and mitochondrial genomes. As such, this snail provides a powerful means to dissect the evolutionary and functional consequences of mito-nuclear variation. The lakes inhabited by P. antipodarum span wide environmental gradients, with substantial across-lake genetic structure and mito-nuclear discordance. This situation allows us to use comparisons across reproductive modes and lakes to partition variation in cellular respiration across genetic and environmental axes. Here, we integrated cellular, physiological, and behavioral approaches to quantify variation in mitochondrial function across a diverse set of wild P. antipodarum lineages. We found extensive across-lake variation in organismal oxygen consumption, mitochondrial membrane potential, and behavioral response to heat stress, but few global effects of reproductive mode or sex. Taken together, our data set the stage for applying this important model system for sexual reproduction and polyploidy to dissecting the complex relationships between mito-nuclear variation, performance, plasticity, and fitness in natural populations.


2020 ◽  
Vol 7 (4) ◽  
pp. 191645
Author(s):  
Anastasia V. Wass ◽  
George Butler ◽  
Tiffany B. Taylor ◽  
Philip R. Dash ◽  
Louise J. Johnson

Tumour evolution depends on heritable differences between cells in traits affecting cell survival or replication. It is well established that cancer cells are genetically and phenotypically heterogeneous; however, the extent to which this phenotypic variation is heritable is far less well explored. Here, we estimate the broad-sense heritability ( H 2 ) of two cell traits related to cancer hallmarks––cell motility and generation time––within populations of four cancer cell lines in vitro and find that motility is strongly heritable. This heritability is stable across multiple cell generations, with heritability values at the high end of those measured for a range of traits in natural populations of animals or plants. These findings confirm a central assumption of cancer evolution, provide a first quantification of the evolvability of key traits in cancer cells and indicate that there is ample raw material for experimental evolution in cancer cell lines. Generation time, a trait directly affecting cell fitness, shows substantially lower values of heritability than cell speed, consistent with its having been under directional selection removing heritable variation.


eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Fabien Duveau ◽  
Petra Vande Zande ◽  
Brian PH Metzger ◽  
Crisandra J Diaz ◽  
Elizabeth A Walker ◽  
...  

Heritable variation in a gene’s expression arises from mutations impacting cis- and trans-acting components of its regulatory network. Here, we investigate how trans-regulatory mutations are distributed within the genome and within a gene regulatory network by identifying and characterizing 69 mutations with trans-regulatory effects on expression of the same focal gene in Saccharomyces cerevisiae. Relative to 1766 mutations without effects on expression of this focal gene, we found that these trans-regulatory mutations were enriched in coding sequences of transcription factors previously predicted to regulate expression of the focal gene. However, over 90% of the trans-regulatory mutations identified mapped to other types of genes involved in diverse biological processes including chromatin state, metabolism, and signal transduction. These data show how genetic changes in diverse types of genes can impact a gene’s expression in trans, revealing properties of trans-regulatory mutations that provide the raw material for trans-regulatory variation segregating within natural populations.


2020 ◽  
Vol 60 (2) ◽  
pp. 275-287
Author(s):  
Emma S Greimann ◽  
Samuel F Ward ◽  
James D Woodell ◽  
Samantha Hennessey ◽  
Michael R Kline ◽  
...  

Synopsis Mitochondrial function is critical for energy homeostasis and should shape how genetic variation in metabolism is transmitted through levels of biological organization to generate stability in organismal performance. Mitochondrial function is encoded by genes in two distinct and separately inherited genomes—the mitochondrial genome and the nuclear genome—and selection is expected to maintain functional mito-nuclear interactions. The documented high levels of polymorphism in genes involved in these mito-nuclear interactions and wide variation for mitochondrial function demands an explanation for how and why variability in such a fundamental trait is maintained. Potamopyrgus antipodarum is a New Zealand freshwater snail with coexisting sexual and asexual individuals and, accordingly, contrasting systems of separate vs. co-inheritance of nuclear and mitochondrial genomes. As such, this snail provides a powerful means to dissect the evolutionary and functional consequences of mito-nuclear variation. The lakes inhabited by P. antipodarum span wide environmental gradients, with substantial across-lake genetic structure and mito-nuclear discordance. This situation allows us to use comparisons across reproductive modes and lakes to partition variation in cellular respiration across genetic and environmental axes. Here, we integrated cellular, physiological, and behavioral approaches to quantify variation in mitochondrial function across a diverse set of wild P. antipodarum lineages. We found extensive across-lake variation in organismal oxygen consumption and behavioral response to heat stress and differences across sexes in mitochondrial membrane potential but few global effects of reproductive mode. Taken together, our data set the stage for applying this important model system for sexual reproduction and polyploidy to dissecting the complex relationships between mito-nuclear variation, performance, plasticity, and fitness in natural populations.


PLoS ONE ◽  
2016 ◽  
Vol 11 (8) ◽  
pp. e0161050 ◽  
Author(s):  
Cristina Takacs-Vesbach ◽  
Kayla King ◽  
David Van Horn ◽  
Katelyn Larkin ◽  
Maurine Neiman

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Gregory R. Keele ◽  
Jeremy W. Prokop ◽  
Hong He ◽  
Katie Holl ◽  
John Littrell ◽  
...  

AbstractChronic kidney disease (CKD), which can ultimately progress to kidney failure, is influenced by genetics and the environment. Genes identified in human genome wide association studies (GWAS) explain only a small proportion of the heritable variation and lack functional validation, indicating the need for additional model systems. Outbred heterogeneous stock (HS) rats have been used for genetic fine-mapping of complex traits, but have not previously been used for CKD traits. We performed GWAS for urinary protein excretion (UPE) and CKD related serum biochemistries in 245 male HS rats. Quantitative trait loci (QTL) were identified using a linear mixed effect model that tested for association with imputed genotypes. Candidate genes were identified using bioinformatics tools and targeted RNAseq followed by testing in a novel in vitro model of human tubule, hypoxia-induced damage. We identified two QTL for UPE and five for serum biochemistries. Protein modeling identified a missense variant within Septin 8 (Sept8) as a candidate for UPE. Sept8/SEPTIN8 expression increased in HS rats with elevated UPE and tubulointerstitial injury and in the in vitro hypoxia model. SEPTIN8 is detected within proximal tubule cells in human kidney samples and localizes with acetyl-alpha tubulin in the culture system. After hypoxia, SEPTIN8 staining becomes diffuse and appears to relocalize with actin. These data suggest a role of SEPTIN8 in cellular organization and structure in response to environmental stress. This study demonstrates that integration of a rat genetic model with an environmentally induced tubule damage system identifies Sept8/SEPTIN8 and informs novel aspects of the complex gene by environmental interactions contributing to CKD risk.


1998 ◽  
Vol 76 (10) ◽  
pp. 1878-1884 ◽  
Author(s):  
Edward P Levri

Foraging behavior can be influenced by such factors as predation risk, individual size, and parasite infection. Snails (Potamopyrgus antipodarum) placed in tanks with large rocks were exposed to four types of water: (1) water with crushed snails, (2) water from a tank in which fish (Gobiomorphus cotidianus) were fed only trout chow, (3) water from a tank where the fish were also fed snails, and (4) plain water. Snails could respond by moving to the top of rocks (where algal food was present) or to the bottom of rocks (where the predation risk was lower). The snails responded to fish chemicals by moving to the bottom of rocks. The response was dependent on snail size and fish diet. Smaller snails moved to the bottom of rocks more than larger snails did. Trematode-infected snails were found on top of the rocks more than other classes of snails, but infected snails still moved to the bottom of rocks in response to the fish predator. Snails eaten by fish in the field tend to be smaller than snails in the overall available population. Thus, snails that are more vulnerable to predation respond more intensely to the odor of fish by moving to the bottom of rocks. This size-dependent response to fish appears to be independent of the occurrence of trematode infection.


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