The influence of aridity on plant intraspecific chemical diversity supports adaptive differentiation and convergent evolution

• Published in: Plant biology (Stuttgart, Germany) Vol. 27; no. 5; pp. 761 - 772
• Main Authors: Castells, E., Sanchez‐Martinez, P.
• Format: Journal Article
• Language: English
• Published: England Wiley Subscription Services, Inc 01.08.2025; John Wiley and Sons Inc
• Subjects: Abiotic factors; Adaptation, Physiological; Adaptive differentiation; Aridity; Biological Evolution; Chemical compounds; Chemical evolution; Controlled conditions; Desert Climate; Differentiation; Environmental gradient; Evolution; evolutionary ecology; Genetic structure; invasive species; Metabolites; Natural selection; neutral markers; plant–climate interactions; Population genetics; Pyrrolizidine alkaloids; Pyrrolizidine Alkaloids - chemistry; Pyrrolizidine Alkaloids - metabolism; Retrorsine; Senecio - chemistry; Senecio - genetics; Senecio - metabolism; Senecio - physiology; Senecio pterophorus; specialized metabolites; Trophic levels; Senecio pterophorus; pyrrolizidine alkaloids; Adaptive differentiation; plant–climate interactions; aridity; evolutionary ecology; specialized metabolites; invasive species; neutral markers
• ISSN: 1435-8603; 1438-8677; 1438-8677
• DOI: 10.1111/plb.13731

Plants synthesize a broad array of specialized chemical compounds that mediate their interactions with the surrounding environment. Some of this chemical diversity is functional and subject to natural selection, but the factors underlying chemical evolution at the intraspecific level remain largely unknown. Here, we combined chemical, environmental and genetic data to investigate the effect of aridity on the expression of chemotypes in the invasive shrub Senecio pterophorus. We studied the variation in pyrrolizidine alkaloids (PAs), a group of specialized metabolites widespread across the families Boraginaceae, Asteraceae and Fabaceae, from native populations spanning a cline of aridity and from three cross‐continental introductions, under natural and common garden conditions. We examined whether the relationship between chemistry and aridity was compatible with a process of adaptive differentiation using a method that partitions the variance and covariance by controlling for the population neutral genetic structure. We found a consistent shift from retrorsine‐like to seneciphylline‐like compounds under increasing aridity in both natural and controlled conditions in coherence with the biosynthetic pathways. This pattern was independent of the neutral genetic structure and occurred along the environmental gradient in the native range and in a convergent manner in all nonnative regions, which suggests adaptive differentiation in response to aridity. Our findings show that the diversity of PAs in S. pterophorus has been partially shaped by aridity. Investigating how abiotic factors influence chemical evolution is key to elucidating the plant responses in future climate scenarios and the cascading effects on other trophic levels. Pyrrolizidine alkaloid composition in the invasive plant Senecio pterophorus is coherent with a pattern of adaptive differentiation in response to aridity, as shown in an environmental gradient in the native range and across three cross‐continental introductions, under natural and common garden conditions, by accounting for the population neutral genetic structure.