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Cellular machinery of energy generation: It is fundamental to all complex lifeforms, but encoded by two different genomes. mtDNA encoded residues are in green, nucDNA encoded residues are in yellow, and residues encoded by one genome that physically interact with the other are in red

​Overview

Most complex lifeforms - humans, animals, plants, and even unicelluar eukaryotes - generate a majortiy of their cellular energy through passing electrons down the electron transport chain, which is composed of protein complexes located in the inner mitochondrial membrane. However, these complexes, and the cellular machinery that is responsible for their transcription and translation, is encoded by two different genomes: the mitochondrial genome, derived from a bacterial progenitor, and the nuclear genome, derived from a different prokaryotic precursor. It is absolutely essential that the intricate interactions between gene products encoded by these two genomes remain in sync. Otherwise, organismal health and fitness decreases drastically.

Exploring the evolution of such cytonuclear interactions has implications for a wide range of topics that are of general interest to biologists. These include the origin of the eukaryotes, endosymbiosis, the ultimate cause of sexual reproduction, why organisms age, how speciation occurs, and environmental adaptation, to name a few. 

Ongoing projects -

 

Mitonuclear coevolution in Silene

Angiosperms in the genus Silene offer unique benefits to studying cytonuclear coevolution because many Silene species retain a slow rate of mtDNA evolution (characteristic of most flowering plants), while some closely related species have undergone massive increases in the rate of mtDNA evolution (as in most animals). Therefore, Silene can be used to examine how the nuclear genome responds to drastic changes in the mitochondrial (and chloroplast) genome. This work is supported by an NIH Postdoctoral Fellowship (F32GM116361)

Some publications describing this work:

Causes and consequences of mito mutations

Mito mutations and speciation

Plastid-nuclear coevolution

Evolution in mito vs. nuclear genomes

Nuclear compensation for mito mutations

Roles of cytoplasmic genomes during speciation

If mutations in cytoplasmic genomes cause the fixation of mutations in the nuclear genome, then cytoplasmic and nuclear genomes might be coadapted to one another within an evolutionary lineage. Hybridization between species or populations might break up these coadapted genomes, leading to hybrid breakdown and reproductive isolation between lineages. Paradoxically, cytoplasmic genomes are especially prone to cross species boundaries. To resolve these conflicting observations, we are using large, publicly available datasets and targeted experiments in Silene to reconcile the contradictory roles for cytoplasmic genomes at species boundaries. 

Some publications describing this work:

The paradoxical roles of cytoplasmic genomes in speciation

Cytonuclear linkage disequilibrium in humans

Mitochondrial mutation pressure and sex

Because both sexual reproduction and mitochondria are only observed in the eukaryotes, but are maintained in nearly all lineages, it is reasonable to assume that the two may be functionally linked. We have hypothesized that mitochondrial mutation pressure may have spurred the evolution of sex. Essentially, when early eukaryotes acquired mitochondrial endosymbionts, their nuclear genomes had to respond to quickly-mutating mitochondrial genomes. Sexual recombination may have arisen in response to selective pressures to coevolve with a quickly-mutating mitochondrial genome. We're excited to test several predictions stemming from this hypothesis using wet lab and bioinformatics approaches.

The publication describing this hypothesis:

A mito-mutation based hypothesis for sex

Mitochondrial function and environmental adaptation

Because mitochondria provide the majority of cellular energy in eukaryotes, mitochondrial function is critical for adaptation to novel environments. We're excited to begin detailed wet lab experiments looking at mitochondrial function in different systems and in different environments. For example, in one ongoing project we're examining how mitochondrial respiration and other phenotypes may change in mountain aquatic insects during acclimation to different thermal environments. We're also hoping to make use of the extremely environmentally variable anchialine ecosystem to see how mitochondrial function in anchialine shrimp might change with salinity. High mitochondrial mutation rates in anchialine shrimps also make them an interesting system to consider mitonuclear coevolution. 

 

Some publications describing previous work in the anchialine ecosystem and other interesting projects: 

Salinity response in anchialine shrimps

Metabolic rates in anchialine shrimps

Mitonuclear basis of gene flow in ancient hominins

Sex, mitochondria, and genetic rescue

Word cloud summarizing research themes from recent publications

Evolutionary relationships in Silene from Havird et al. 2017 GBE

Models of mitonuclear epistasis that could lead to reproductive isolation from Sloan et al. 2017 Mol Ecol

Click herehere, and here for some popular press coverage of our mito-mutation and sex hypothesis

Baetis spp. from the Rockies, acclimated to high temp

Example high resolution respirometry from aquatic insect mitochondria coupled with various substrates

H. rubra from the Hawaiian anchialine ecosystem

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