Biology subjects

Healy, T. M.

Publications and source records attributed to Healy, T. M..

7 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↗

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↗

bioRxiv2018

Conserved patterns of alternative splicing in response to cold acclimation in fish

Phenotypic plasticity is an important aspect of an organisms response to environmental change that often requires the modulation of gene expression. These changes in gene expression can be quantitative as a result of increases or decreases in the amounts of specific transcripts, or qualitative as a result of the expression of alternative transcripts from the same gene (e.g., via alternative splicing of pre-mRNAs). Although the role of quantitative changes in gene expression in phenotypic plasticity is well known, relatively few studies have examined the role of qualitative changes. Here, we use skeletal muscle RNA-seq data from Atlantic killifish (Fundulus heteroclitus), threespine stickleback (Gasterosteus aculeatus) and zebrafish (Danio rerio) to investigate the extent of qualitative changes in gene expression in response to cold. Fewer genes demonstrated alternative splicing than differential expression as a result of cold acclimation; however, differences in splicing were detected for between 426 and 866 genes depending on species, indicating that large numbers of qualitative changes in gene expression are associated with cold acclimation. Many of these alternatively spliced genes were also differentially expressed, and there was functional enrichment for involvement in muscle contraction among the genes demonstrating qualitative changes in response to cold acclimation. Additionally, there was a common group of 29 genes with cold-acclimation-mediated changes in splicing in all three species, suggesting that there may be a conserved set of genes with expression patterns that respond qualitatively to prolonged cold temperatures across fishes.\n\nSummary statementQualitative changes in gene expression, such as those mediated by alternative splicing of mRNAs, are involved in phenotypic plasticity in response to prolonged cold acclimation in ectothermic animals

zoology↗

bioRxiv2018

Genome-wide selection scans integrated with association mapping reveal mechanisms of physiological adaptation across a salinity gradient in killifish

Adaptive divergence between marine and freshwater environments is important in generating phyletic diversity within fishes, but the genetic basis of adaptation to freshwater habitats remains poorly understood. Available approaches to detect adaptive loci include genome scans for selection, but these can be difficult to interpret because of incomplete knowledge of the connection between genotype and phenotype. In contrast, genome wide association studies (GWAS) are powerful tools for linking genotype to phenotype, but offer limited insight into the evolutionary forces shaping variation. Here, we combine GWAS and selection scans to identify loci important in the adaptation of complex physiological traits to freshwater environments. We focused on freshwater (FW)-native and brackish water (BW)-native populations of the Atlantic killifish (Fundulus heteroclitus) as well as a population that is a natural admixture of these two populations. We measured phenotypes for multiple physiological traits that differ between populations and that may contribute to adaptation across osmotic niches (salinity tolerance, hypoxia tolerance, metabolic rate, and body shape) and used a reduced representation approach for genome-wide genotyping. Our results show patterns of population divergence in physiological capabilities that are consistent with local adaptation. Selection scans between BW-native and FW-native populations identified genomic regions that presumably aect fitness between BW and FW environments, while GWAS revealed loci that contribute to variation for each physiological trait. There was substantial overlap in the genomic regions putatively under selection and loci associated with the measured physiological traits, suggesting that these phenotypes are important for adaptive divergence between BW and FW environments. Our analysis also implicates candidate genes likely involved in physiological capabilities, some of which validate a priori hypotheses. Together, these data provide insight into the mechanisms that enable diversification of fishes across osmotic boundaries.\n\nAuthor SummaryIdentifying the genes that underlie adaptation is important for understanding the evolutionary process, but this is technically challenging. We bring multiple lines of evidence to bear for identifying genes that underlie adaptive divergence. Specifically, we integrate genotype-phenotype association mapping with genome-wide scans for signatures of natural selection to reveal genes that underlie phenotypic variation and that are adaptive in populations of killifish that are diverging between marine and freshwater environments. Because adaptation is likely manifest in multiple physiological traits, we focus on hypoxia tolerance, salinity tolerance, and metabolic rate; traits that are divergent between marine and freshwater populations. We show that each of these phenotypes is evolving by natural selection between environments; genetic variants that contribute to variation in these physiological traits tend to be evolving by natural selection between marine and freshwater populations. Furthermore, one of our top candidate genes provides a mechanistic explanation for previous hypotheses that suggest the adaptive importance of cellular tight junctions. Together, these data demonstrate a powerful approach to identify genes involved in adaptation and help to reveal the mechanisms enabling transitions of fishes across osmotic boundaries.

evolutionary biology↗