Range-wide study in a sexually polymorphic wild strawberry reveals climatic and soil associations of sex ratio, sexual dimorphism, and sex chromosomes

Authors: Cullen, Nevin; RICHARDSON, ETHAN - University Of Pittsburgh; BUDINSKY, TREZALKA - University Of Pittsburgh; REEB, RACHEL - Carnegie Museum Of Natural History; MORTIMER, SEBASTIAN - Oregon State University; LISTON, AARON - Oregon State University; ASHMAN, TIA-LYNN - University Of Pittsburgh

Submitted to: Journal of Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/19/2024
Publication Date: 4/28/2024
Citation: Cullen, N.P., Richardson, E.T., Budinsky, T.A., Reeb, R.A., Mortimer, S.M., Liston, A., Ashman, T. 2024. Range-wide study in a sexually polymorphic wild strawberry reveals climatic and soil associations of sex ratio, sexual dimorphism, and sex chromosomes. Journal of Ecology. https://doi.org/10.1111/1365-2745.70056.
DOI: https://doi.org/10.1111/1365-2745.70056

Interpretive Summary: We investigated landscape scale influences driving bias in sex ratios, sexual dimorphism and sex chromosomal variation in the wild strawberry, Fragaria virginiana, a subdioecious species (populations have hermaphrodites, males and females) that is broadly distributed across North America. We used ~7000 digitized herbarium and iNaturalist specimens to understand how sex ratio varies with geographic, climatic and soil gradients in wild strawberries. We found that availability of soil resources dictated sex ratio, but in opposite patterns in Eastern and Western North America. For example, in eastern populations, soil nitrogen was negatively correlated with female bias, while in western populations, soil nitrogen was positively correlated with female bias. We also found that female plants were more likely to reproduce sexually (via flowers) and asexually (via runners) at the same time than males, though males increased their likelihood of producing runners under climatic stress (cold winter temperatures and high latitudes). We additionally used tissue from ~300 herbarium specimens to understand the distribution of the three different sex determining types across their range. Here, we discovered the frequency of sex determining types is associated with soil moisture and precipitation.

Technical Abstract: 1. Climatic and soil features influence resources and mate availability for plants. Because of different resource/mating demands of the male and female reproductive pathways, environmental variation can drive geographic patterns of sex-specific factors in sexually polymorphic species. Yet, the relationship between environment and sex, sexual dimorphism or sex chromosomes at the range-wide scale is underexamined. 2. Using ~7,000 herbarium and iNaturalist specimens we generate a landscape-scale understanding of how sex ratio and sexual dimorphism vary with geographic, climatic and soil gradients in the sexually polymorphic wild strawberry (Fragaria virginiana) and test whether these conform to predictions from theory. Then, for ~300 specimens we use genotyping of the sex-determining region (SDR haplotypes) to reveal geographic and phenotypic pattens in sex chromosome types. 3. Across North America, sex ratio was hermaphrodite/male-biased and was associated more with soil attributes than climate. Sex ratio-environment associations matched 16 predictions for subdioecy in the West but for gynodioecy in the East. Climatic factors correlated with sexual dimorphism in traits related to carbon acquisition (leaf size and runnering while flowering) but not mate access (petal size, flowering time). Variation in sexual dimorphism was due to one sex being more responsive to the environmental variation than the other. Specifically, leaf length in females was more responsive to variation in precipitation than in hermaphrodite/males, but the probability of runnering while flowering in hermaphrodite/males was more responsive to variation in temperature than in females. The ancestral sex chromosome type was most common overall. But the frequency of the more derived sex chromosomes varied with environmental factors that differed between East-West regions. Synthesis: A landscape-level perspective revealed that variation in soil and 27 climate factors can explain geospatial variation in sex ratio and sexual dimorphism in a wild strawberry. Variation in sex ratio was associated more with soil resources than climate, while variation in sexual dimorphism was the result of sex-differential responses to climate for vegetative traits but similar response to abiotic factors in mate access traits. Finally, sex chromosome types were associated with soil moisture and precipitation in ways that could contribute to the evolution of sex determination.