Ecological Predictors of Organelle Genome Evolution: Phylogenetic Correlations with Taxonomically Broad, Sparse, Unsystematized Data

Abstract

Comparative analysis of variables across phylogenetically linked observations can reveal mechanisms and insights in evolutionary biology. As the taxonomic breadth of the sample of interest increases, challenges of data sparsity, poor phylogenetic resolution, and complicated evolutionary dynamics emerge. Here, we investigate a cross-eukaryotic question where all these problems exist: which organismal ecology features are correlated with gene retention in mitochondrial and chloroplast DNA (organelle DNA or oDNA). Through a wide palette of synthetic control studies, we first characterize the specificity and sensitivity of a collection of parametric and non-parametric phylogenetic comparative approaches to identify relationships in the face of such sparse and awkward datasets. This analysis is not directly focused on oDNA, and so provides generalizable insights into comparative approaches with challenging data. We then combine and curate ecological data coupled to oDNA genome information across eukaryotes, including a new semi-automated approach for gathering data on organismal traits from less systematized open-access resources including encyclopedia articles on species and taxa. The curation process also involved resolving several issues with existing datasets, including enforcing clade-specificity of several ecological features and fixing incorrect annotations. Combining this unique dataset with our benchmarked comparative approaches, we confirm support for several known links between organismal ecology and organelle gene retention, identify several previously unidentified relationships constituting possible ecological contributors to oDNA genome evolution, and provide support for a recently hypothesized link between environmental demand and oDNA retention. We, with caution, discuss the implications of these findings for organelle evolution and of this pipeline for broad comparative analyses in other fields.

Evolution and maintenance of mtDNA gene content across eukaryotes

“…We found that the same features of hydrophobicity, GC content, and energetic centrality predict cpDNA gene retention as well as mtDNA retention -and, strikingly, this prediction is quantitative in the sense that a model trained on mtDNA retention profiles predicts cpDNA retention profiles (Giannakis, Arrowsmith, et al, 2022). The theory developed suggesting that strong and dynamic environmental demands favour organelle gene retention also applies to cpDNA (García-Pascual et al, 2022), and we observed consistencies among environmental features statistically linked with gene retention profiles in both organelles (Giannakis et al, 2024). Indeed, a weak but robust correlation between mtDNA and cpDNA gene counts is detectable in the subset of species for which records are available for both (Giannakis, Richards, et al, 2023).…”

“…This theory predicts semi-quantitatively that more oDNA encoding is advantageous in organisms subject to strong, variable environmental demands, while nuclear transfer is advantageous in stable, less demanding environments. This is supported by a cross-taxa phylogenetic comparative investigation of mtDNA gene count and ecology (Giannakis et al, 2024). Here, attempting to account for the difficulty of comparisons across the broad, sparse, uncertain datasets available, we found fewer genes retained in organelles exposed to limited demands (endoparasites, and plastids without photosynthetic demands) and more genes in those exposed to more varying environments (in sessile organisms, deserts, and tropical oceans).…”

“…Across kingdoms, parasitism is often associated with reduced gene content (Giannakis et al, 2024); in an extreme example, a cnidarian parasite retaining mitochondria but lacking mtDNA has been reported (Yahalomi et al, 2020).…”

“…1B inset). Strong, dynamic environmental changes favour gene retention for CoRR (Allen, 2015;García-Pascual et al, 2022;Giannakis et al, 2024). Maintaining mtDNA heterozygosity to adapt to changing environments may also influence which inheritance patterns are favoured (Radzvilavicius & Johnston, 2020, 2022.…”

The nitroplast and its relatives support a universal model of features predicting gene retention in endosymbiont and organelle genomes

“…The retained subset of genes in organelles and endosymbionts varies dramatically across eukaryotes, and the features favouring gene retention are not completely understood (Butenko et al, 2024;García-Pascual et al, 2022;Giannakis et al, 2023Giannakis et al, , 2024McCutcheon & Moran, 2012;Smith & Keeling, 2015). Hypotheses have often focused on mitochondria and plastids, and have included roles for hydrophobicity (making it harder for nuclear-encoded genes to be imported to the organelle (Björkholm et al, 2015;von Heijne, 1986)); favouring local individual control of organelles (colocalization for redox regulation or CoRR (Allen, 2015)); the economics of maintaining and expressing genes from diFerent compartments (Kelly, 2021), and others (quantitatively compared in (Giannakis et al, 2022)).…”