How evolution repeatedly builds complexity: a case study with C photosynthesis in Blepharis (Acanthaceae).

Résumé

With over 60 parallel origins representing evolutionary replicates, C photosynthesis is well-suited for studying complex trait evolution. However, lineages with diverse C-C intermediate species are scarce, leaving uncertainty in models of C evolution. Phenotypic characterization of 28 living species of Blepharis (Acanthaceae) is presented, including photosynthetic gas exchange, enzyme activity assays, cell ultrastructure, and δC assays, the latter including 92 herbarium specimens from three species with phenotypic diversity. A well-resolved transcriptome-based phylogeny provides evolutionary context. C, proto-Kranz, C, C-like, and C phenotypes occur in Blepharis sect. Acanthodium. The phylogeny supports a stepwise progression from C through C to C states and up to five distinct origins of the C cycle. Substantial intraspecific C-C variation is demonstrated in Blepharis mitrata, Blepharis furcata, and Blepharis macra. Blepharis gazensis is a monospecific C lineage exhibiting an NADP malic enzyme C pathway with features of the NAD-ME subtype, extending the ways in which the C cycle is known to function. Substantial photosynthetic diversity exists in Blepharis that rivals or exceeds the range of character states present in other C to C transitional lineages. This diversity in Blepharis represents a robust new model for studying convergent evolution of C photosynthesis and complex traits in general.