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.