C4 anatomy can evolve via a single developmental change.

C4 photosynthesis is a complex trait that boosts productivity in warm environments. Paradoxically, it evolved independently in numerous plant lineages, despite requiring specialised leaf anatomy. The anatomical modifications underlying C4 evolution have previously been evaluated through interspecific comparisons, which capture numerous changes besides those needed for C4 functionality. Here, we quantify the anatomical changes accompanying the transition between non-C4 and C4 phenotypes by sampling widely across the continuum of leaf anatomical traits in the grass Alloteropsis semialata. Within this species, the only trait that is shared among and specific to C4 individuals is an increase in vein density, driven specifically by minor vein development that yields multiple secondary effects facilitating C4 function. For species with the necessary anatomical preconditions, developmental proliferation of veins can therefore be sufficient to produce a functional C4 leaf anatomy, creating an evolutionary entry point to complex C4 syndromes that can become more specialised.

Population-Specific Selection on Standing Variation Generated by Lateral Gene Transfers in a Grass.

Evidence of eukaryote-to-eukaryote lateral gene transfer (LGT) has accumulated in recent years [1-14], but the selective pressures governing the evolutionary fate of these genes within recipient species remain largely unexplored [15, 16]. Among non-parasitic plants, successful LGT has been reported between different grass species [5, 8, 11, 16-19]. Here, we use the grass Alloteropsis semialata, a species that possesses multigene LGT fragments that were acquired recently from distantly related grass species [5, 11, 16], to test the hypothesis that the successful LGT conferred an advantage and were thus rapidly swept into the recipient species. Combining whole-genome and population-level RAD sequencing, we show that the multigene LGT fragments were rapidly integrated in the recipient genome, likely due to positive selection for genes encoding proteins that added novel functions. These fragments also contained physically linked hitchhiking protein-coding genes, and subsequent genomic erosion has generated gene presence-absence polymorphisms that persist in multiple geographic locations, becoming part of the standing genetic variation. Importantly, one of the hitchhiking genes underwent a secondary rapid spread in some populations. This shows that eukaryotic LGT can have a delayed impact, contributing to local adaptation and intraspecific ecological diversification. Therefore, while short-term LGT integration is mediated by positive selection on some of the transferred genes, physically linked hitchhikers can remain functional and augment the standing genetic variation with delayed adaptive consequences.