Heterochrony underpins natural variation in Cardamine hirsuta leaf form

Significance A key problem in biology is whether the same processes underlie morphological variation between and within species. Here, we show that the causes of leaf shape diversity at these two evolutionary scales can be divergent. Some species have simple leaves, whereas others bear complex leaves comprising leaflets. Previous work indicated that these interspecific differences result mostly from variation in local tissue growth and patterning. Now we find that a different process, age-dependent shape progression, underlies within-species variation in complex leaf morphology. Specifically, in plants with accelerated aging and early flowering, leaves progress to adult shapes with more leaflets, faster than their slower-aging counterparts. This mechanism coordinates leaf development with reproductive timing and may influence resource allocation to seeds. A key problem in biology is whether the same processes underlie morphological variation between and within species. Here, by using plant leaves as an example, we show that the causes of diversity at these two evolutionary scales can be divergent. Some species like the model plant Arabidopsis thaliana have simple leaves, whereas others like the A. thaliana relative Cardamine hirsuta bear complex leaves comprising leaflets. Previous work has shown that these interspecific differences result mostly from variation in local tissue growth and patterning. Now, by cloning and characterizing a quantitative trait locus (QTL) for C. hirsuta leaf shape, we find that a different process, age-dependent progression of leaf form, underlies variation in this trait within species. This QTL effect is caused by cis-regulatory variation in the floral repressor ChFLC, such that genotypes with low-expressing ChFLC alleles show both early flowering and accelerated age-dependent changes in leaf form, including faster leaflet production. We provide evidence that this mechanism coordinates leaf development with reproductive timing and may help to optimize resource allocation to the next generation.