Intraorganismal genetic heterogeneity as a source of genetic variation in modular macroalgae

Abstract

Genetic diversity is considered a key factor of population survival and evolution, especially in changing environments. Genetic diversity arises from mutations in the DNA sequence of cell lines and from there it reaches the level of organisms, populations, and regions. However, many previous studies have not considered the organism architecture or pattern of thallus construction, ignoring the potential genetic complexities that intraorganismal genetic heterogeneity could generate in modular organisms. In seaweeds, modularity and clonality exist in many species. Modular organization has been related to advantages in terms of rapid construction and recovery after the loss of individual modules, which have their own demographic properties as they generate, mature, senesce, and die. Based on recent evidence from the literature, we suggest that modules also have their own genetic properties. Specifically, modular seaweeds have two possible sources of genetic diversity at the individual level: the heterozygosity of the genotypes composing the genet, and genetic heterogeneity among the modules within a genet (i.e., intraclonal genetic variability). Both sources of genetic diversity can have ecological and evolutionary consequences, and most of them must be considered in research on modular seaweeds. Linking intraorganismal genetic diversity with clonal architecture and propagation styles may help us to understand important ecological and evolutionary processes such as speciation modes, invasive capacities, or farming potential.

The Seagrass Methylome Is Associated With Variation in Photosynthetic Performance Among Clonal Shoots

“…Independent from genetic variation was also the methylome shift in the experimental samples that provides potential for temporally stable phenotypic change at time scales unattainable by somatic mutations. Particularly across mitotically grown generations, epigenetic patterns can be expected to be more faithfully inherited than across sexual generations, because clonal growth circumvents epigenetic reprogramming during meiosis and embryogenesis (Santelices et al, 2018;Simberloff and Leppanen, 2019;Yu et al, 2020). Thus, our results provide a first indication that DNA methylation variation provides a layer of ecologically relevant phenotypic variation that is independent from genetic variation in clonal seagrass meadows.…”

Somatic genetic drift and multi-level selection in modular species

“…Whether or not the identified inter-module genetic differentiation translates into different phenotypes is an open and highly intriguing question 4,12,13,19,47 . Experimental studies have revealed differences in physiological performance among asexually propagating modules of clonal plants and algal thalli 10,17,18,20 , suggesting the principal significance of inter-module phenotypic selection. We suggest that somatic genetic drift producing inter-module genetic differentiation will apply to many clonally proliferating species, providing an additional source of genetic variation for adaptation.…”

“…In line with this notion, population genetic models have demonstrated that with increasing longevity, there may be far more mitotic cell divisions during one zygote cycle than meiotic ones 14 , potentially providing large mutational input for both, selection and somatic genetic drift to operate 15,16 . Accordingly, several studies have demonstrated the emergence of phenotypic differences among modules of the same genet 10,17,18 . However, the corresponding genome-level assessments of frequency, dynamics and possible functional consequences 19,20 of somatic genetic variation are currently lacking for any modular species.…”

Evolution via somatic genetic variation in modular species

“…Evidence from plant invasions [56], agricultural breeding via asexual propagation [57], direct experimentation of hereditary variation within clonal lineages [54,58,59]; and the very interesting cases of transmissible cancer [60] suggest a substantial potential for asexual adaptation under multi-cellularity. Given that many clonal species are at the same time ecosystem foundation species [61][62][63], studying this alternative route of adaptive evolution is highly relevant to conservation and ecological genetics [30].…”