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SummaryPlant volatile emissions can recruit predators of herbivores for indirect defence and attract pollinators to aid in pollination. Although volatiles involved in defence and pollinator attraction are primarily emitted from leaves and flowers, respectively, they will co-evolve if their underlying genetic basis is intrinsically linked, either due to pleiotropy or genetic linkage. However, direct evidence of co-evolving defence and floral traits is scarce.We characterized intra-specific variation of herbivory-induced plant volatiles (HIPVs), the key components of indirect defence against herbivores, and floral volatiles in the wild tobacco Nicotiana attenuata.We found that variation of (E)-β-ocimene and (E)-α-bergamotene contributed to the correlated changes in HIPVs and floral volatiles among N. attenuata natural accessions. Intra-specific variations of (E)-β-ocimene and (E)-α-bergamotene emissions resulted from allelic variation of two genetically co-localized terpene synthase genes, NaTPS25 and NaTPS38 respectively.Analyzing haplotypes of NaTPS25 and NaTPS38 revealed that allelic variations of NaTPS25 and NaTPS38 resulted in correlated changes of (E)-β-ocimene and (E)-α-bergamotene emission in HIPVs and floral volatiles in N. attenuata.Together, these results provide evidence that pleiotropy and genetic linkage result in correlated changes in defences and floral signals in natural populations, and the evolution of plant volatiles is likely under diffuse selection.

Functional variation is known to influence population yield, but the scale at which this happens is still unknown. Relevant signals might only reach immediate neighbors of a phenotypically diverse plant (neighbor-scale) or conversely may distribute across the population (population-scale). We useNicotiana attenuatasilenced in mitogen-activated protein kinase 4 (irMPK4), plants with low water-use efficiency (WUE), to study the scale at which water-use traits alter intraspecific population yields. In the field and glasshouse, populations with low percentages of irMPK4 plants planted among isogenic control plants produced maximum overall growth and yield. Through paired-plant and local-plant-configuration analyses, we determined that this occurred at the population scale. However, we find that this effect was not due to irMPK4’s WUE phenotype. With micro-grafting, we additionally show thatMPK4-deficiency may mediate the response at the population-scale: shoot-expressedMPK4is required forN. attenuatato change yield in response to a neighbor.