Clonal conundrum, part deux



In the second installment of the clonal conundrum, one hallmark of clonality is one that surprisingly hasn’t been validated that many times using species that have both sexually and asexually reproducing populations. Theoretically, clonal reproduction should generate massive …

Heterozygote excess

Mutations accumulate in clonal lineages as the two alleles at each locus irreversibly diverge within individuals (Balloux et al. 2003). This should generate largely negative Fis values. As clonality increases, Fis decreases:

Figure 1 from Balloux et al. 2003: Fis as a function of the rate of clonal reproduction. The line represents analytical results and the solid circles simulation results.

Figure 1 from Balloux et al. (2003): Fis as a function of the rate of clonal reproduction. The line represents analytical results and the solid circles simulation results.

Balloux et al. (2003) suggest that strict clonality can, thus, be easily detected in populations due to the excess of heterozygotes. But, the occurrence of sex, even infrequently, what they term cryptic sex, might also be detected. Fis values will be variable among loci:
Figure 2 from Balloux et al. (2003). Standard errors of Fis as a function of the rate of clonal reproduction.

Figure 2 from Balloux et al. (2003). Standard errors of Fis as a function of the rate of clonal reproduction.

Halkett et al. (2005) were interested in exploring the existence of gene flow between sexual and asexual lineages and to quantify its importance in aphids.
Rhopalosiphum padi ©

Rhopalosiphum padi ©

Indeed, heterozygote excess was inversely proportional to the frequency of sexual reproduction (e.g., Simon et al. 1999, Halkett et al. 2005).
Table 5 from Halkett et al. (2005)

Table 5 from Halkett et al. (2005)

As demonstrated in Balloux et al. (2003), Halkett et al. (2005) found variance among Fis values.

Both predictions match the present data set [Halkett et al. 2005], suggesting that ‘facultatively asexuals’ mostly reproduce asexually, and that there is a very limited input from sexual reproduction episodes to the ‘facultatively asexual’ cluster.

Guillemin et al. (2008) have contributed to the overall list of organisms for which these predictions are applicable. In G. chilensis, farmed populations not only had loads of repeated genotypes, but also had significantly negative Fis values!
Yet, more studies in organisms with sexual and asexual populations are warranted.
But, unlike aphids or higher plants, there are two free-living phases in haploid and diploid stages.

Gracilaria life cycle © SA Krueger-Hadfield

Gracilaria life cycle © SA Krueger-Hadfield

This leads to an additional signature of clonality which is only applicable to haploid-diploid organisms:

Uncoupling of haploid-diploid life cycles

In the case of seaweeds, like G. chilensis, clonal propagation has led to artificial selection of diploid individuals. Diploids tend to grow faster in Gracilaria species (Guillemin et al. 2013) and this is what farmers want.

Within a few decades, [there has been] massive replication of clonal individuals that can cover hectares of high-density biomass [in G. chilensis farms]. This is equivalent of a very high number of generations of clonal propagation for each single genotype.

Guillemin et al. (2008) found one farmed population that included both haploid and diploid thalli and they found significant differences in allele frequencies between the haploid and diploid phases.
This pattern is not unlike two distinct, but isolated populations diverging from one another via genetic drift. Sexual reproduction links the haploid and diploid phases together such that there should be no differences in allele frequencies.
Sosa et al. (1998) found a similar pattern in a different species of red macroalgae, Gelidium arbuscula. However, the lack of differences between the haploid and diploid phases has suggested the occurrence of sex, even if just enough to yield similar allele frequencies, in several other algal studies (e.g., Coyer et al. 1994, van der Strate et al. 2002, Engel et al. 2004, Krueger-Hadfield et al. 2013).
In all of the aphid and algal examples above, asexual populations were also characterized by increased linkage disequilibrium …
Balloux F, Lehmann L, de Meeus T (2003) The population genetics of clonal and partially clonal diploids. Genetics, 164, 1635– 1644.
Coyer, JA, DL Robertson, and RS Alberte (1994) Genetic variability within a population and between diploid/haploid tissue of Macrocystis pyrifera (Phaeophyceae). Journal of Phycology, 30, 545–552.
Engel, CR, C Destombe, and M Valero (2004) Mating system and gene flow in the red seaweed Gracilaria gracilis: effect of haploid-diploid life history and intertidal rocky shore landscape on fine scale genetic structure. Heredity 92:289–298.
Guillemin ML, Faugeron S, Destombe C, et al. (2008) Genetic variation in wild and cultivated populations of the haploid-diploid red alga Gracilaria chilensis: How farming practices favor asexual reproduction and heterozygosity. Evolution, 62, 1500–1519.
Guillemin M-L, Sepulveda RD, Correa JA & Destombe C (2013) Differential ecological responses to environmental stress in the life history phases of the isomorphic red alga Gracilaria chilensis (Rhodophyta). Journal of Applied Phycology, 25, 215-224.
Halkett, F., J.-C. Simon, and F. Balloux (2005) Tackling the population genet- ics of clonal and partially clonal organisms. TREE 20:194– 201.
Krueger-Hadfield, SA, D Roze, S Mauger and M Valero (2013) Intergametophytic selfing and microgeographic genetic structure shape populations of the intertidal red seaweed Chondrus crispus.  Molecular Ecology 222: 3242-3260.
Simon, JC, S Baumann, P Sunnucks, PDN Hebert, JS Pierre, JF Le Gallic, and CA Dedryver (1999) Reproductive mode and population genetic structure of the cereal aphid Sitobion avenae studied using phenotypic and microsatellite markers. Molecular Ecology 8, 531–545.

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