Quantitative genetics of phosphorus content in the freshwater herbivore, Daphnia pulicaria

Abstract

Phosphorus (P) is essential for growth of all organisms, and P content is correlated with growth in most taxa. Although P content was initially considered to be a trait fixed at the species level, there is growing evidence for considerable intraspecific variation. Selection on such variation can thus alter the rates at which P fluxes through food webs. Nevertheless, prior work describing the sources and extent of intraspecific variation in P content were not genetically explicit, confounded by unknown genetic background and evolutionary history. We constructed an F2 recombinant population of the dominant freshwater grazer, Daphnia pulicaria to mitigate such issues. F2 recombinants exhibited considerable variation in growth rate, P content (0.49%–1.97%), P use efficiency (PUE; 51–208 mg biomass/mg P), and correlated traits such as hatching time of resting eggs, in common garden conditions. These results clearly demonstrate the scope of genetic recombination in generating variation in ecologically relevant traits. The absence of environmental selection is a likely component driving such variation not observed in natural settings. Although phosphoglucose isomerase (PGI) genotype was significantly associated with variation in hatching time of resting eggs, contrary to prior work with less rigorous designs, and allelic variation at the PGI locus did not explain variation in P content and PUE of Daphnia, indicating that such quantitative traits are under polygenic control. Together, these results suggest that although there is considerable genetic scope for variation in key ecologically relevant traits, such as P content and efficiency of P use, these traits are likely under strong stabilizing selection, most likely due to selection on growth rate and size. Importantly, our observations suggest that anthropogenic alterations to P supply due to eutrophication could alter selection on these traits, thereby rapidly altering the role Daphnia plays in the P cycle of lakes.

Eutrophication‐driven eco‐evolutionary dynamics indicated by differences in stoichiometric traits among populations of Daphnia pulicaria

“…Across our study lakes, Daphnia populations in P‐rich lakes increasingly comprised Pgi‐ heterozygotes, which exhibit lower production and P‐use efficiency (Jeyasingh et al., 2009). While allozyme variants in Pgi predict varying performance in Daphnia (Jeyasingh et al., 2009; Weider et al., 1997) and other invertebrates (Wheat, 2010), variation at Pgi alone does not fully explain phenotypic variation and differential fitness of Daphnia observed in this study (Sherman et al., 2021). Notably, eutrophic source populations in the 60 μg/L TP mesocosms and 425 μg/L TP mesocosms exhibited similar trends in prevalence of Pgi ‐homozygotes, but the variance among individual mesocosms also was quite high.…”

“…Whether such a combination of traits is biologically possible is unclear, but the persistence of Daphnia from the eutrophic Green Castle Lake across all treatments in the mesocosm experiment is consistent with this hypothesis. Alternatively, genetic variation within populations could explain how Daphnia perform well across a spectrum of dietary phosphorus (Sherman et al., 2021). Further phylogeographic work examining population structure across the landscape and heterogeneity within lakes will reveal important insights about how lakes will respond to eutrophication or restoration.…”

“…Standing genetic variation in D . pulicaria allows for varying performance with food quality (Sherman et al., 2021), and it is therefore not surprising that Daphnia populations from hypereutrophic lakes have adapted to optimize performance under these conditions. While models such as that developed by Peace et al.…”

“…In Daphnia , two alleles of Pgi are common: the fast allele (referred to as allele 4) which migrates faster than the slow allele (referred to as allele 1) during electrophoresis (Carvalho, 1988). Since Pgi appears to exhibit overdominance in that homozygotes at either allele produce phosphoglucose isomerase proteins with similar properties and similar variation in P‐use efficiency relative to those produced by heterozygotes (Boriss, 2001; Orsini et al., 2009; Sherman et al., 2021), we defined homozygotes as those with a 1–1 or 4–4 genotype. All heterozygotes had a 1–4 genotype.…”

“…Further supporting the importance of considering variation in reaction norm shape, Daphnia populations from the mesocosm experiments varied over a similar range of dry biomass to the lakes surveyed across Iowa, but reached peak mean biomass in the TP treatments corresponding to their respective source lakes. Standing genetic variation in D. pulicaria allows for varying performance with food quality (Sherman et al, 2021), and it is therefore not surprising that Daphnia populations from hypereutrophic lakes have adapted to optimize performance under these conditions. While models such as that developed by Peace et al (2013) are useful for understanding mechanistic processes that alter population dynamics, they must be interpreted with caution when being applied to natural populations.…”