Skip to main content
Dryad logo

Exploring the genetic consequences of clonality in haplodiplontic taxa

Citation

Krueger-Hadfield, Stacy et al. (2020), Exploring the genetic consequences of clonality in haplodiplontic taxa, Dryad, Dataset, https://doi.org/10.5061/dryad.djh9w0vzh

Abstract

Partially clonality is an incredibly common reproductive mode found across all the major eukaryotic lineages. Yet, population genetic theory is based on exclusive sexuality or exclusive asexuality and partial clonality is often ignored. This is particularly true in haplodiplontic eukaryotes, including algae, ferns, mosses, and fungi, where somatic development occurs in both the haploid and diploid stages. Haplodiplontic life cycles are predicted to be correlated with asexuality, but tests of this prediction are rare. Moreover, there are unique consequences of having long-lived haploid and diploid stages in the same life cycle. For example, clonal processes uncouple the life cycle such that the repetition of the diploid stage via clonality leads to the loss of the haploid stage. Here, we surveyed the literature to find studies that had genotyped both haploid and diploid stages and re-calculated population genetic summary metrics for seven red algae, one green alga, three brown algae, and three mosses. We compared these data to recent simulations that explicitly addressed the population genetic consequences of partial clonality in haplodiplontic life cycles. Not only was partial clonality found to act as a homogenizing force, but the combined effects of proportion of haploids, rate of clonality, and the relative strength of mutation versus genetic drift impacts the distributions of population genetic indices. We found remarkably similar patterns across commonly used population genetic metrics between our empirical and recent theoretical expectations. To facilitate future studies, we provide some recommendations for sampling and analyzing population genetic parameters for haplodiplontic taxa.

Methods

Re-analysis of haplodiplontic genetic data to test similarities between theoretical predictions and empirical data from:

Publications:

Couceiro L, Le Gac M, Hunsperger HM et al. (2015a) Evolution and maintenance of haploid-diploid life cycles in natural populations: The case of the marine brown alga Ectocarpus. Evolution, 69, 1808–1822.

Engel CR, Destombe C, Valero M (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 M-L, 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.

Hutsemékers V, Hardy OJ, Vanderpoorten A (2013) Does water facilitate gene flow in spore-producing plants? Insights from the fine-scale genetic structure of the aquatic moss Rhynchostegium riparioides (Brachytheciaceae). Aquatic Botany, 108, 1–6.

Krueger-Hadfield SA (2011) Structure des populations chez l’algue rouge haploid-diploïde Chondrus crispus: système de reproduction, différeciation génétique et épidémiologie. PhD Thesis, Université de Pierre et Marie Curie Sorbonne Universités and Pontificia Universidad Católica de Chile. 375pp.

Krueger-Hadfield SA, Roze D, Mauger S, Valero M (2013) Intergametophytic selfing and microgeographic genetic structure shape populations of the intertidal red seaweed Chondrus crispus. Molecular Ecology, 22, 3242–3260.

Krueger-Hadfield SA, Kollars NM, Byers JE et al. (2016a) Invasion of novel habitats uncouples haplo-diplontic life cycles. Molecular Ecology, 25, 3801–3816.

Krueger-Hadfield SA, Kollars NM, Strand AE et al. (2017) Genetic identification of source and likely vector of a widespread marine invader. Ecology and Evolution, 7, 4432–4447.

Pardo C, Guillemin ML, Pena V et al. (2019a) Local coastal configuration rather than latitudinal gradient shape clonal diversity and genetic structure of Phymatolithon calcareum maerl beds in North European Atlantic. Frontiers in Marine Science, 6, 149.

Rosengren F, Cronberg N, Hansson B (2016) Balance between inbreeding and outcrossing in a nannandrous species, the moss Homalothecium lutescens. Heredity, 116, 107–113.

Sosa PA, Valero M, Batista F, Gonzalez-Perez MA (1998) Genetic variation and genetic structure of natural populations of Gelidium species: A re-evaluation of results. Journal of Applied Phycology, 10, 279–284.

Steen F, Marc V, D’Hondt S, Vieira C, Clerck OD (2019) Population structure and geographically structured reproductive strategies of the haplodiplontic seaweed Dictyota dichotoma. bioRxiv, 40, 95–39. https://doi.org/10.1101/595587

van der Strate HJ, van de zande L, Stam WT, Olsen JL (2002) The contribution of haploids, diploids and clones to fine-scale population structure in the seaweed Cladophoropsis membranacea (Chlorophyta). Molecular Ecology, 11, 329–345.

van der Velde M, During HJ, van de Zande L, Bijlsma RK (2001) The reproductive biology of Polytrichum formosum: clonal structure and paternity revealed by microsatellites. Molecular Ecology, 10, 2423–2434.

Dryad Datasets:

Couceiro L, Le Gac M, Hunsperger HM et al. (2015b) Data from: Evolution and maintenance of haploid-diploid life cycles in natural populations: The case of the marine brown alga Ectocarpus. Dryad Dataset https://doi.org/10.5061/dryad.391dj

Krueger-Hadfield SA, Kollars NM, Byers JE et al. (2016b) Data from: Invasion of novel habitats uncouples haplo-diplontic life cycles. Dryad Dataset https://doi.org/10.5061/dryad.fg818.

Krueger-Hadfield SA et al. (2018a), Data from: Genetic identification of source and likely vector of a widespread marine invader. Dryad dataset, https://doi.org/10.5061/dryad.fn53k

Krueger-Hadfield SA et al. (2012), Data from: Intergametophytic selfing and microgeographic genetic structure shape populations of the intertidal red seaweed Chondrus crispus. Dryad, Dataset, https://doi.org/10.5061/dryad.751p3

Pardo C, Guillemin ML, Pena V et al. (2019b) Data from: Local coastal configuration rather than latitudinal gradient shape clonal diversity and genetic structure of Phymatolithon calcareum maerl beds in North European Atlantic. Dryad Dataset https://doi.org/10.5061/dryad.ds2714g

Rosengren F, Cronberg N, Hansson B (2015) Data from: Balance between inbreeding and outcrossing in a nannandrous species, the moss Homalothecium lutescens. Dryad, Dataset, https://doi.org/10.5061/dryad.1860s

Usage Notes

Table S1. An excel spreadsheet of organism (red alga, brown alga, green alga, or moss), marker type (allozyme, microsatellite, SNP), site, species, ploidy (1 = haploid, 2 = diploid), and allele information for each locus (haploids have one allele and diploids have two alleles).

Table S2. Single - and mutlilocus population genetic metrics.

Date Sheet – Indices

Marker: marker type (allozyme, microsatellite, SNP); species (see Table 1); pop (site); R overall (genotypic richness); BetaPareto overall (pareto ß); Beta_score_hap (haploid score); clonality in haploids (clonal rate in diploids low, mid or high); N haploids (number of haploids); proportionofhaploidsval (actual haploid proportion); Proportion of haploids (binned haploid proportion); R haploids (genotypic richness in haploids); BetaPareto haploids (pareto ß in the haploids); rbarDAR haploids (rd in the haploids); SWinx haploids (genotypic evenness in haploids); pidst haploids (identity between sibs in haploids); MHe haploids (mean HE); varHe haploids (variance in HE in haploids); Beta_score_dip (pareto ß score in diploids); clonality in diploids (clonal rate in diploids – low, mid, or high); N diploids (number of diploids); R diploids (genotypic richness in diploids); BetaPareto diploids (pareto ß in diploids); rbarDAR diploids (rd in the diploids); SWinx diploids (genotypic evenness in diploids); pidst diploids (identity between sibs in diploids);); MHe diploids (mean HE in diploids); varHe diploids (variance in HE in diploids); MFIS diploids (mean FIS); VARFIS (variance in FIS); MHo (mean HO); varHo (variance in HO); Fst between haploids and diploids (FST between haploid and diploid subpopulations).

Data Sheet – All pops

phylum; species (see Table 1); pop (site); ploidy (1: haploid; 2: diploid); N (sample size); G (number of unique genotypes); R (genotypic richness); BetaPareto (pareto ß); rbarDAR (rd); Swinx (genotypic evenness); pidst (identity between sibs); MHe (mean HE); varHe (variance in HE); MFIS (mean FIS); VARFIS (variance in FIS); MHo (mean HO); varHo (variance in HO).

Sheet – Clonal ranking for plots

species (see table 1); clonality in haploids (low, mid, or high based on pareto ß); BetaPareto (pareto ß); median of pareto beta (median pareto ß for the species); mean of pareto beta (mean pareto ß for the species); ranking from highest to least clonal (1: most clonal; 14: least clonal)

Funding

College of Arts and Sciences, University of Alabama at Birmingham, Award: Start-Up Funds

Agence Nationale de la Recherche, Award: Clonix2D ANR-18-CE32-0001