Neopolyploidy increases stress tolerance and reduces fitness plasticity across multiple urban pollutants: support for the "general-purpose" genotype hypothesis

Abstract

Whole-genome duplication is a common macromutation with extensive impacts on gene expression, cellular function, and whole-organism phenotype. As a result, it has been proposed that polyploids have "general-purpose" genotypes that perform better than their diploid progenitors under stressful conditions. Here, we test this hypothesis in the context of stresses presented by anthropogenic pollutants. Specifically, we tested how multiple neotetraploid genetic lineages of the mostly asexually reproducing greater duckweed (Spirodela polyrhiza) perform across a favorable control environment and 5 urban pollutants (iron, salt, manganese, copper, and aluminum). By quantifying the population growth rate of asexually reproducing duckweed over multiple generations, we found that across most pollutants, but not all, polyploidy decreased the growth rate of actively growing propagules but increased that of dormant ones. Yet, when considering total propagule production, polyploidy increased tolerance to most pollutants, and polyploids maintained population-level fitness across pollutants better than diploids. Furthermore, broad-sense genetic correlations in growth rate among pollutants were all positive in neopolyploids but not so for diploids. Our results provide a rare test and support for the hypothesis that polyploids are more tolerant of stressful conditions and can maintain fitness better than diploids across heterogeneous stresses. These results may help predict that polyploids may be likely to persist in stressful environments, such as those caused by urbanization and other human activities.

Keywords: Lemnaceae; autopolyploidy; environmental trade-off; genetic correlation; urban ecology; urban evolution.

Figure 1.

Daily frond population growth rates (estimated marginal means ± 1 SE) separated by ploidy and genetic lineage (including an overall average) across the six pollutant treatments (including the control). The table above shows the percentage difference of neopolyploid (4×) in relation to diploid (2×), along with the p-values resulting from the six planned contrasts between diploids and neotetraploids for each pollutant treatment averaged across all lineages. Point positions were dodged for clarity, with circles representing diploids and triangles representing neotetraploids.

Figure 2.

Total turion production (estimated marginal means ± 1 SE) separated by ploidy and genetic lineage (including an overall average) across the six pollutant treatments (including the control). The table above shows the percentage difference of neopolyploid (4×) in relation to diploid (2×), along with the p-values resulting from the six planned contrasts between diploids and neotetraploids for each pollutant treatment. Point positions were dodged for clarity, with circles representing diploids and triangles representing neotetraploids.

Figure 3.

Tolerance of each pollutant (stressor/control, estimated marginal means ± 1 SE) combining frond and turion growth across ploidy and genetic lineage (including an overall average). Tolerance values of 1 imply no impact of stressors on fitness. The table above shows the percentage difference of neopolyploid (4×) in relation to diploid (2×), along with the p-values resulting from the five planned contrasts between diploids and neotetraploids for each pollutant. Point positions were dodged for clarity, with circles representing diploids and triangles representing neotetraploids.

Figure 4.

Plasticity in fitness across all pollutants (excluding the control) for each lineage and ploidy. Plasticity, quantified as the Relative Distance Plasticity Index (RDPI) of growth rates, combining fronds and turions, among the five pollutants. Values of 0 imply complete fitness maintenance (no plasticity) and 1 imply maximum plasticity. Post hoc Tukey HSD test results are shown above each lineage pair.

Figure 5.

Broad-sense genetic correlations of population growth rate between pairs of pollutant environments (excluding the control). The lower triangle of the matrix includes Pearson’s correlations for diploids and the upper triangle for tetraploids. p-values < .075 are shown. Positive (negative) correlations are in blue (red) with a darker shade reflecting the strength of the correlation.