The discernible and hidden effects of clonality on the genotypic and genetic states of populations: improving our estimation of clonal rates

Abstract

Partial clonality is widespread across the tree of life, but most population genetics models are designed for exclusively clonal or sexual organisms. This gap hampers our understanding of the influence of clonality on evolutionary trajectories and the interpretation of population genetics data. We performed forward simulations of diploid populations at increasing rates of clonality (c), analysed their relationships with genotypic (clonal richness, R, and distribution of clonal sizes, Pareto β) and genetic (FIS and linkage disequilibrium) indices, and tested predictions of c from population genetics data through supervised machine learning. Two complementary behaviours emerged from the probability distributions of genotypic and genetic indices with increasing c. While the impact of c on R and Pareto β was easily described by simple mathematical equations, its effects on genetic indices were noticeable only at the highest levels (c>0.95). Consequently, genotypic indices allowed reliable estimates of c, while genetic descriptors led to poorer performances when c<0.95. These results provide clear baseline expectations for genotypic and genetic diversity and dynamics under partial clonality.Worryingly, however, the use of realistic sample sizes to acquire empirical data systematically led to gross underestimates (often of one to two orders of magnitude) of c, suggesting that many interpretations hitherto proposed in the literature, mostly based on genotypic richness, should be reappraised. We propose future avenues to derive realistic confidence intervals for c and show that, although still approximate, a supervised learning method would greatly improve the estimation of c from population genetics data.

Genomic signatures of clonality in the deep water kelp Laminaria rodriguezii

“…The identification of repeated MLGs in addition to mean negative values of F IS , and significant linkage disequilibrium across loci observed in L. rodriguezii are features that all agree with signatures of clonality in natural populations (Balloux et al, 2003;. Nevertheless, we must be aware that inferring the rates of clonality by taking into account both the genotypic richness (R) and the average F IS values remains unachievable, except for high levels of clonality, greater than 95% (Balloux et al, 2003;Stoeckel et al, 2019), or requires the availability of temporal samples (Ali et al, 2016;Becheler et al, 2017). Furthermore, the estimates of R are strongly dependent on sampling strategy and density, basically decreasing with increasing sampling effort (Arnaud-Haond et al, 2007;Becheler et al, 2017;Gorospe et al, 2015).…”

“…Furthermore, the estimates of R are strongly dependent on sampling strategy and density, basically decreasing with increasing sampling effort (Arnaud-Haond et al, 2007;Becheler et al, 2017;Gorospe et al, 2015). In that context, recent studies reported that R had poor relevance for measuring the relative importance of sexual versus clonal reproduction (Arnaud-Haond et al, 2019), even using relatively large sample sizes (from 100 to 500 individuals) (Stoeckel et al, 2019). Therefore, we suspect that the genotypic richness (R) of L. rodriguezii was probably overestimated in our study, due to the complexity of sampling at these depths (i.e.…”

“…However, by looking at the F IS distribution in the genome, we propose a new analysis which seems useful to detect partial clonal reproduction. F IS rather than R is considerably less sensitive to sampling density (Arnaud-Haond et al, 2019;Stoeckel et al, 2019), thus its distribution could be used for detecting genomic signatures of clonal reproduction. Furthermore, inter-locus variance of F IS (rather than an average value) was predicted to increase as clonal rates increase (Balloux et al, 2003;Stoeckel & Masson 2014;Reichel et al, 2016;Stoeckel et al, 2019).…”

“…F IS rather than R is considerably less sensitive to sampling density (Arnaud-Haond et al, 2019;Stoeckel et al, 2019), thus its distribution could be used for detecting genomic signatures of clonal reproduction. Furthermore, inter-locus variance of F IS (rather than an average value) was predicted to increase as clonal rates increase (Balloux et al, 2003;Stoeckel & Masson 2014;Reichel et al, 2016;Stoeckel et al, 2019). Further investigations showed that the distribution of F IS along genomes is expected to be concentrated between -0.3 and 0.1 under intermediate levels of clonality, while strongly shifted to negative values for high levels of clonality (Stoeckel & Masson, 2014).…”

“…strong selection, automixis) may shape the genetic composition of asexual organisms. More generally, apart from the rate of asexual reproduction, the genetic diversity of partially clonal populations is evidently shaped by the interaction of reproductive mode with genetic drift, gene flow, and mutation (Stoeckel & Masson, 2014;Reichel et al, 2016;Stoeckel et al, 2019). Indeed, mathematical models have predicted that such evolutionary forces can lead to specific patterns of distribution of F IS over the genome, characterized by a high occurrence of extreme values, mainly negative (Stoeckel & Masson, 2014;Reichel et al, 2016).…”