Rate of clonality
In line with the definition summarised above, the rate of clonality (here, c ) corresponds to “…the probability of clonality versus sexual reproduction through selfing or outcrossing ” (Marshall & Weir, 1979), which in this article corresponds to the ratio of the effective number of descendants produced by clonality to the total effective number of descendants produced in a population (see also Balloux, Lehmann, & de Meeus, 2003; Berg & Lascoux, 2000).
When inferred by genotypic and genetic indices in a population sample, this rate is a proxy for the idealised number of descendants produced by clonality relative to the total idealised number of descendants produced in the population that would result in the same genotypic and genetic effects.
Despite the prevalence of PC and the potential extent of its consequences at the ecosystem level, the consequences of PC for the evolution of species and the ecological dynamics of their natural populations have been subject to little in-depth theoretical or empirical development (Yonezawa, Ishii, & Nagamine, 2004). This lack of development makes a substantial number of studies on partially clonal species confusing when analysing population genetics data and interpreting them in terms of demographic and evolutionary dynamics (Avise, 2015; Fehrer, 2010; Yu et al., 2016). Nevertheless, the effects of PC are likely to be extremely important at all spatial and temporal scales. For example, evolutionarily speaking, the ability of a given genotype to persist across generations adds a new target for natural selection, namely, the genotype (Ayala, 1998).
Three main knowledge gaps are related to PC: diagnosing it in species where its occurrence is not obviously inferred by classical naturalistic observations (e.g. , human pathogens, in contrast to rhizomatic clonal plants); quantifying its extent once a given species is determined to be partially clonal; and understanding its influence on the ecological and evolutionary trajectories of partially clonal species by investigating their population genetics. These gaps have been only partly filled during the past 30 years. The use of molecular markers in a population genetics framework paved the way for easier detection of PC (De Meeûs, Lehmann, & Balloux, 2006; Halkett, Simon, & Balloux, 2005; Tibayrenc, Kjellberg, & Ayala, 1990) through the discrimination of clonal lineages and detailed analysis of the genotypic and genetic compositions of species suspected of having PC (Arnaud-Haond et al., 2005; Bailleul, Stoeckel, & Arnaud-Haond, 2016; Tibayrenc et al., 1990). However, conditions allowing (or not allowing) the detection of PC and its consequences for the trajectories of natural populations over different time scales are likely important yet still poorly understood (Avise, 2015; Dia et al., 2014; Fehrer, 2010; Yu et al., 2016). We still face difficulties in inferring the rate of clonal (denoted c ) versus sexual (1-c ) reproduction or an approximate but consistentproxy for it (i.e. , the “level of clonality”). These difficulties prevent access to the empirical information necessary to compare the ecological dynamics and evolutionary trajectories of partially clonal populations living in different environments (McMahon et al., 2017). To understand the effect of PC on the fate of natural populations and species, the value of c should first be estimated.
The rate of clonality in natural populations may be estimated by tracking clonal spreads or determining groups of clones. In plants, groups of clones have sometimes been identified at local scales through extremely time-consuming and tedious mark-recapture studies of rhizomes (Eckert, 2002; Marbà & Duarte, 1998). However, using this method on large spatial scales and for most species exhibiting PC through fragmentation or multiplication at microscopic stages is unrealistic. Therefore, tracking clonal spread or determining groups of clones through population genetics is the only solution for the vast majority of species. Unfortunately, although population genetics studies can illuminate the occurrence of PC in nature, no method has been developed thus far to reliably infer (or at least estimate) such potentially crucial parameters in natural populations using indices gathered through a classical one-time step sampling strategy. Two recently developed methods allow the quantification of rates of clonality in populations genotyped at two time steps. However, they require sampling the population twice at an interval of at least one generation and, more importantly, a comprehensive knowledge of major life history traits, such as generation time, which are seldom available except for well-known macroscopic species for which extensive field data have been collected (Ali et al., 2016; Becheler et al., 2017).
Most empirical studies thus infer the importance of clonal reproduction in populations using a one-time step sampling strategy to compute the ratio of genotypes to the number of sampling units (genotypic richness,\(Pd=G/N\)) as an estimate of clonal richness. Genotypic richness is often implicitly assumed to have a linear relationship with the rate of sexual reproduction \(1-c\) and to be comparable among natural populations submitted to the same sampling strategy. Theoretical studies have shown the strong influence of high clonality rates (c>0.95) alone on parameters such asF IS and linkage disequilibrium (LD ) (Balloux et al., 2003; De Meeûs et al., 2006; Navascués, Stoeckel, & Mariette, 2010) but no noticeable departure from expectations under purely sexual reproduction at lower rates of clonality. However, more recent mathematical developments have shown that the distribution ofF IS is wider at high clonality rates but is actually affected at all clonality rates (Stoeckel & Masson, 2014), depending on the strength of departure from equilibrium (Reichel, Masson, Malrieu, Arnaud-Haond, & Stoeckel, 2016).
This research led to a present-day paradox in the literature on PC. Many populations exhibit average or elevated genotypic diversity, leading several authors to conclude that these populations exhibit a high incidence of sexual reproduction, whereas in the same studies, consistent departure from Hardy-Weinberg equilibrium (HWE), when reported (which is much rarer), would instead have led them to conclude that the populations exhibit a negligible occurrence of sexual recombination versus clonal reproduction (e.g., Orantes, Zhang, Mian, & Michel, 2012; Villate, Esmenjaud, Van Helden, Stoeckel, & Plantard, 2010). This paradox is seldom obvious because F ISvalues are often not reported or, if reported, are not interpreted in relation to clonality. In any case, part of this paradox may lie in the pervasive effect of sampling on the estimation of genotypic richness (Arnaud-Haond, Duarte, Alberto, & Serrão, 2007; Gorospe, Donahue, & Karl, 2015). These two studies demonstrated this worrying effect by using two empirical datasets (of seagrasses and corals) where the true rates of clonality were unknown; assessing the order of magnitude of these rates thus requires further investigation.