Phylogenomics in Cactaceae: A case study using the chollas sensu lato (Cylindropuntieae, Opuntioideae) reveals a common pattern out of the Chihuahuan and Sonoran deserts.

Premise: Although numerous phylogenetic studies have been conducted in Cactaceae, whole-plastome datasets have not been employed. We used the chollas to develop a plastome dataset for phylogeny reconstruction to test species relationships, biogeography, clade age, and morphological evolution.

Methods: We developed a plastome dataset for most known diploid members of the chollas (42 taxa) as well as for other members of Cylindropuntieae. Paired-end, raw reads from genome skimming were reference-mapped onto a de novo plastome assembly of one species of cholla, Cylindropuntia bigelovii, and were used to build our plastome dataset, which was analyzed using various methods.

Results: Our plastome dataset resolved the phylogeny of the chollas, including most interspecific and intraspecific relationships. Tribe Cylindropuntieae arose ~18 mya, during the early Miocene in southern South America, and is supported as sister to the South American clade Tephrocacteae. The (Micropuntia (Cylindropuntia + Grusonia)) clade most likely originated in the Chihuahuan Desert region around 16 mya and then migrated into other North American desert regions. Key morphological characters for recognizing traditional taxonomic series in Cylindropuntia (e.g., spiny fruit) are mostly homoplasious.

Conclusions: This study provides the first comprehensive plastome phylogeny for any clade within Cactaceae. Although the chollas s.l. are widespread throughout western North American deserts, their most recent common ancestor likely arose in the Chihuahuan Desert region during the mid-Miocene, with much of their species diversity arising in the early to mid-Pliocene, a pattern strikingly similar to those found in other western North American desert groups.