6Pgdh polymorphism in wild bulb mite populations: prevalence, environmental correlates and life history trade-offs

Abstract

Genetic polymorphism in key metabolic genes plays a pivotal role in shaping phenotypes and adapting to varying environments. Polymorphism in the metabolic gene 6-phosphogluconate dehydrogenase (6Pgdh) in bulb mites, Rhizoglyphus robini is characterized by two alleles, S and F, that differ by a single amino acid substitution and correlate with male reproductive fitness. The S-bearing males demonstrate a reproductive advantage. Although the S allele rapidly fixes in laboratory settings, the persistence of polymorphic populations in the wild is noteworthy. This study examines the prevalence and stability of 6Pgdh polymorphism in natural populations across Poland, investigating potential environmental influences and seasonal variations. We found widespread 6Pgdh polymorphism in natural populations, with allele frequencies varying across locations and sampling dates but without clear geographical or seasonal clines. This widespread polymorphism and spatio-temporal variability may be attributed to population demography and gene flow between local populations. We found some correlation between soil properties, particularly cation content (Na, K, Ca, and Mg) and 6Pgdh allele frequencies, showcasing the connection between mite physiology and soil characteristics and highlighting the presence of environment-dependent balancing selection. We conducted experimental fitness assays to determine whether the allele providing the advantage in male-male competition has antagonistic effects on life-history traits and if these effects are temperature-dependent. We found that temperature does not differentially influence development time or juvenile survival in different 6Pgdh genotypes. This study reveals the relationship between genetic variation, environmental factors, and reproductive fitness in natural bulb mite populations, shedding light on the dynamic mechanisms governing 6Pgdh polymorphism.

Keywords: Rhizoglyphus robini; 6-Phosphogluconate dehydrogenase; Balancing selection; Genetic polymorphism; Genotype–environment interaction for fitness; Metabolic gene.

Fig. 1

Methods of laboratory fitness assays—a Development time, b Juvenile survival

Fig. 2

F-allele frequency of natural bulb mite populations at different locations in Poland in spring

Fig. 3

F-allele frequencies between spring and autumn at various locations in Poland

Fig. 4

a The results from the PCA showing the PC1 and PC2 axes explaining 44.3% and 19.8% of the variance in soil patterns respectively. b The inverse relationship of the second PC axis with the Na, Mg, K and Ca content of the soil. Units: S (%), P (%), organic matter (%), Na (mg kg⁻¹), N (%), Mn, Mg, K, Ca (mg kg⁻¹), C (%). All data are expressed per dry soil mass. c Negative relationship between PC2 and F-allele frequency

Fig. 5

a Development time for bulb mites with different genotypes of the 6Pgdh allele at different temperatures. The boxplot shows the median along with the interquartile range. The points represent the spread of individual data points. b F-allele frequencies of the juveniles that survived at each temperature. The boxplot shows the median along with the interquartile range. The data points represent the F-frequency of the replicates