Biology subjects

Burton, R. S.

Publications and source records attributed to Burton, R. S..

6 recordsLinked to original sources

bioRxiv2022

Genetic incompatibilities in reciprocal hybrids between populations of Tigriopus californicus with low to moderate mitochondrial sequence divergence

All mitochondrial-encoded proteins and RNAs function through interactions with nuclear-encoded proteins. These interactions are critical for mitochondrial function and eukaryotic fitness, and coevolution maintains inter-genomic (i.e., mitonuclear) compatibility within taxa. Hybridization can disrupt coevolved interactions, resulting in hybrid breakdown, and mitonuclear incompatibilities may be important mechanisms underlying reproductive isolation and, potentially, speciation. Recently, signatures of strong selection to maintain compatible mitonuclear genotypes in hybrids have been detected in at least some inter-population crosses. However, this work has only been conducted in crosses between populations with extremely high levels of genetic divergence in both their mitochondrial and nuclear genomes, leaving the generality of strong selection for mitonuclear compatibility unclear. Here we address this limitation with reciprocal inter-population F2 hybrids between relatively low-divergence populations of the intertidal copepod Tigriopus californicus. Our results show that the dominance of mitonuclear effects consistent with coevolved mitonuclear genotypes in fast-developing (i.e., high-fitness) hybrids is reduced in low-divergence crosses, but that selection to maintain mitonuclear compatibility is still observed on some nuclear chromosomes. Consequently, we demonstrate that, even at low levels of genetic divergence between taxa, mitonuclear incompatibilities may play a key role in the early stages of reproductive isolation.

evolutionary biology↗

bioRxiv2022

Developmental rate displays effects of inheritance but not of sex in inter-population hybrids of Tigriopus californicus

Coevolved interactions between mitochondrial-encoded and nuclear-encoded genes within populations can be disrupted by inter-population hybridization resulting in reduced hybrid fitness. This hybrid breakdown may be an important factor contributing to reproductive isolation between populations or species, and strong selection among hybrids to maintain compatible mitonuclear genotypes occurs in at least some species. Despite potentially differential consequences of mitonuclear incompatibilities in females and males due to maternal inheritance of the mitochondrial genome, the extent to which phenotypic variation associated with hybrid breakdown is sex-specific and heritable remains unresolved. Here we present two experiments investigating variation in developmental rate among reciprocal inter-population hybrids of the intertidal copepod Tigriopus californicus. Developmental rate is a proxy for fitness in this species that is substantially influenced by variation in mitonuclear compatibility among hybrids. First, we show that F2 hybrid developmental rate is the same in females and males, suggesting that effects of mitonuclear incompatibilities on this trait are likely experienced equally by the two sexes. Second, we demonstrate that variation in developmental rate among F3 hybrids is heritable; times to copepodid metamorphosis of F4 offspring of fast-developing F3 parents (12.25 {+/-} 0.05 d, {+/-} SEM) were significantly faster than those of F4 offspring of slow-developing parents (14.58 {+/-} 0.05 d). Taken together, these results provide evidence for strong effects of mitonuclear interactions across generations of hybrid eukaryotes with no differences between the sexes, and support key roles of mitonuclear incompatibility in hybrid breakdown and reproductive isolation.

evolutionary biology↗

bioRxiv2022

Differential gene expression and mitonuclear incompatibilities in fast- and slow-developing inter-population Tigriopus californicus hybrids

Mitochondrial functions are intimately reliant on proteins and RNAs encoded in both the nuclear and mitochondrial genomes, leading to inter-genomic coevolution within taxa. Hybridization can break apart coevolved mitonuclear genotypes, resulting in decreased mitochondrial performance and reduced fitness. This hybrid breakdown is an important component of outbreeding depression and early-stage reproductive isolation. However, the mechanisms contributing to mitonuclear interactions remain poorly resolved. Here we scored variation in developmental rate (a proxy for fitness) among reciprocal F2 inter-population hybrids of the intertidal copepod Tigriopus californicus, and used RNA sequencing to assess differences in gene expression between fast- and slow-developing hybrids. In total, differences in expression associated with developmental rate were detected for 2,925 genes, whereas only 135 genes were differentially expressed as a result of differences in mitochondrial genotype. Up-regulated expression in fast developers was enriched for genes involved in chitin-based cuticle development, oxidation-reduction processes, hydrogen peroxide catabolic processes and mitochondrial respiratory chain complex I. In contrast, up-regulation in slow developers was enriched for DNA replication, cell division, DNA damage and DNA repair. Eighty-four nuclear-encoded mitochondrial genes were differentially expressed between fast- and slow-developing copepods, including twelve subunits of the electron transport system (ETS) which all had higher expression in fast developers than in slow developers. Nine of these genes were subunits of ETS complex I. Our results emphasize the major roles that mitonuclear interactions within the ETS, particularly in complex I, play in hybrid breakdown, and resolve strong candidate genes for involvement in mitonuclear interactions.

evolutionary biology↗

bioRxiv2022

Phenotypic and transcriptional response of Daphnia pulicaria to the combined effects of temperature and predation

Daphnia, an ecologically important zooplankton species in lakes, shows both genetic adaptation and phenotypic plasticity in response to temperature and fish predation, but little is known about the molecular basis of these responses and their potential interactions. We performed a factorial experiment exposing laboratory-propagated Daphnia pulicaria clones from two lakes in the Sierra Nevada mountains of California to normal or high temperature (15{degrees}C or 25{degrees}C) in the presence or absence of fish kairomones, then measured changes in life history and gene expression. Exposure to kairomones increased upper thermal tolerance limits for physiological activity in both clones. Cloned individuals matured at a younger age in response to higher temperature and kairomones, while size at maturity, fecundity and population intrinsic growth were only affected by temperature. At the molecular level, both clones expressed more genes differently in response to temperature than predation, but specific genes involved in metabolic, cellular, and genetic processes responded differently between the two clones. Although gene expression differed more between clones from different lakes than experimental treatments, similar phenotypic responses to predation risk and warming arose from these clone-specific patterns. Our results suggest that phenotypic plasticity responses to temperature and kairomones interact synergistically, with exposure to fish predators increasing the tolerance of Daphnia pulicaria to stressful temperatures, and that similar phenotypic responses to temperature and predator cues can be produced by divergent patterns of gene regulation.

ecology↗

bioRxiv2019

Interactions across life stages and thermal tolerance plasticity in Tigriopus californicus

In response to rapid environmental change, organisms rely on both genetic adaptation and phenotypic plasticity to adjust key traits that are necessary for survival and reproduction. Given the accelerating rate of climate change, plasticity may be particularly important. For organisms in warming aquatic habitats, upper thermal tolerance is likely to be a key trait, and many organisms express plasticity in this trait in response to developmental or adulthood temperatures. Although plasticity at one life stage may influence plasticity at another life stage, relatively little is known about these interactive effects for thermal tolerance. Here we used locally adapted populations of the intertidal copepod Tigriopus californicus to investigate these interactions in a marine ectotherm. We found that low latitude populations had greater critical thermal maxima (CTmax) than high latitude populations, and variation in developmental temperature altered CTmax plasticity in adulthood. After development at 25{degrees}C, CTmax was plastic in adults, whereas no adult plasticity in this trait was observed after 20{degrees}C development. This pattern was identical across four populations, suggesting that local thermal adaptation has not shaped this interactive effect. However, differences in the capacities to maintain ATP synthesis rates and to induce heat shock proteins at high temperatures, two likely mechanisms of local adaptation in this species, were consistent with changes in CTmax due to developmental temperatures, suggesting there is mechanistic overlap between plastic interactions and adaptation in general. These results indicate that interactive effects of plasticity across life stages may have substantial impacts on upper thermal tolerance in ectothermic organisms.\n\nSummary statementDevelopmental temperatures alter the plasticity of thermal limits in adults of a marine ectotherm, and differences in ATP synthesis rate and heat shock protein expression parallel the changes in tolerance.

zoology↗

bioRxiv2019

Mitochondrial DNA has strong selective effects across the nuclear genome

Oxidative phosphorylation requires gene products encoded in both the nuclear and mitochondrial genomes, and is the primary source of cellular energy in eukaryotes. As a result, functional integration between the genomes is essential for efficient ATP generation in these organisms. Although within populations this integration is presumably maintained by coevolution, both the importance of coevolution in speciation and mitochondrial disease, and the strength of selection for maintenance of coevolved genotypes are widely questioned. In this study, we crossed populations of the intertidal copepod, Tigriopus californicus, to disrupt putatively coevolved mitonuclear genotypes in reciprocal F2 hybrids. We utilized inter-individual variation in developmental rate, a proxy for fitness, among these hybrids to assess the strength of selection imposed on the nuclear genome by alternate mitochondrial genotypes. There was substantial variation in developmental rate among hybrid individuals, and in vitro ATP synthesis rates of mitochondria isolated from high fitness hybrids were approximately twice those of mitochondria isolated from low fitness individuals. Furthermore, we used Pool-seq to reveal large deviations in nuclear allele frequencies in hybrids, which favored maternal alleles in only high fitness individuals of each reciprocal cross. Therefore, our most fit hybrids had partial recovery of coevolved genotypes, indicating that mitonuclear effects underlie individual-level variation in developmental rate and that inter-genomic compatibility is critical for high fitness. These results demonstrate that mitonuclear interactions have profound impacts on both physiological performance and the evolutionary trajectory of the nuclear genome.

evolutionary biology↗