Genome-wide patterns of selection-drift variation strongly associate with organismal traits across the green plant lineage [RESEARCH]

Kavitha Uthanumallian1, Andrea Del Cortona2, Susana M. Coelho3, Olivier De Clerck2, Sebastian Duchene4,5 and Heroen Verbruggen1,6 1Melbourne Integrative Genomics, School of BioSciences, University of Melbourne, Parkville VIC 3010, Australia; 2Department of Biology, Phycology Research Group, Ghent University, 9000 Ghent, Belgium; 3Department of Algal Development and Evolution, Max Planck Institute for Developmental Biology, 72076 Tübingen, Germany; 4Department of Microbiology and Immunology, Peter Doherty Institute for Infection and Immunity, University of Melbourne, Parkville VIC 3010, Australia; 5Department of Computational Biology, Institut Pasteur, 75015 Paris, France; 6CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado, Campus de Vairão, Universidade do Porto, 4485-661 Vairão, Portugal Corresponding authors: kuthanumallistudent.unimelb.edu.au, heroenunimelb.edu.au Abstract

There are many gaps in our knowledge of how life cycle variation and organismal body architecture associate with molecular evolution. Using the diverse range of green algal body architectures and life cycle types as a test case, we hypothesize that increases in cytomorphological complexity are likely to be associated with a decrease in the effective population size, because larger-bodied organisms typically have smaller populations, resulting in increased drift. For life cycles, we expect haploid-dominant lineages to evolve under stronger selection intensity relative to diploid-dominant life cycles owing to masking of deleterious alleles in heterozygotes. We use a genome-scale data set spanning the phylogenetic diversity of green algae and phylogenetic comparative approaches to measure the relative selection intensity across different trait categories. We show stronger signatures of drift in lineages with more complex body architectures compared with unicellular lineages, which we consider to be a consequence of smaller effective population sizes of the more complex algae. Significantly higher rates of synonymous as well as nonsynonymous substitutions relative to other algal body architectures highlight that siphonous and siphonocladous body architectures, characteristic of many green seaweeds, form an interesting test case to study the potential impacts of genome redundancy on molecular evolution. Contrary to expectations, we show that levels of selection efficacy do not show a strong association with life cycle types in green algae. Taken together, our results underline the prominent impact of body architecture on the molecular evolution of green algal genomes.

Footnotes

[Supplemental material is available for this article.]

Article published online before print. Article, supplemental material, and publication date are at https://www.genome.org/cgi/doi/10.1101/gr.279002.124.

Freely available online through the Genome Research Open Access option.

Received January 17, 2024. Accepted August 16, 2024.

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