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

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.