Adaptation to a new environment with pre‐adaptive genomic features – Evidence from woody plants colonizing the land–sea interface

SUMMARY Adaptation to new environments is a key evolutionary process which presumably involves complex genomic changes. Mangroves, a collection of approximately 80 woody plants that have independently invaded intertidal zones >20 times, are ideal for studying this process. We assembled near‐chromosome‐scale genomes of three Xylocarpus species as well as an outgroup species using single‐molecule real‐time sequencing. Phylogenomic analysis reveals two separate lineages, one with the mangrove Xylocarpus granatum and the other comprising a mangrove Xylocarpus moluccensis and a terrestrial Xylocarpus rumphii. In conjunction with previous studies, we identified several genomic features associated with mangroves: (i) signals of positive selection in genes related to salt tolerance and root development; (ii) genome‐wide elevated ratios of non‐synonymous to synonymous substitution relative to terrestrial relatives; and (iii) active elimination of long terminal repeats. These features are found in the terrestrial X. rumphii in addition to the two mangroves. These genomic features, not being strictly mangrove‐specific, are hence considered pre‐adaptive. We infer that the coastal but non‐intertidal habitat of X. rumphii may have predisposed the common ancestor to invasion of true mangrove habitats. Other features including the preferential retention of duplicated genes and intolerance to pseudogenization are not found in X. rumphii and are likely true adaptive features in mangroves. In conclusion, by studying adaptive shift and partial shifts among closely related species, we set up a framework to study genomic features that are acquired at different stages of the pre‐adaptation and adaptation to new environments. Significance Statement We sequenced and assembled high‐quality genomes for three Xylocarpus species and one Swietenia species using single‐molecule real‐time sequencing. By illustrating genomic features acquired in different stages of the complex process of adapting to the extreme intertidal environments, we provide evidences for pre‐adaptation and adaptation in different stages of transition to a new environment