Origin and Diversification of the Saguaro Cactus (Carnegiea gigantea): A Within-Species Phylogenomic Analysis

Abstract

Reconstructing accurate historical relationships within a species poses numerous challenges, not least in many plant groups in which gene flow is high enough to extend well beyond species boundaries. Nonetheless, the extent of tree-like history within a species is an empirical question on which it is now possible to bring large amounts of genome sequence to bear. We assess phylogenetic structure across the geographic range of the saguaro cactus, an emblematic member of Cactaceae, a clade known for extensive hybridization and porous species boundaries. Using 200 Gb of whole genome resequencing data from 20 individuals sampled from 10 localities, we assembled two data sets comprising 150,000 biallelic single nucleotide polymorphisms (SNPs) from protein coding sequences. From these we inferred within-species trees and evaluated their significance and robustness using five qualitatively different inference methods. Despite the low sequence diversity, large census population sizes, and presence of wide-ranging pollen and seed dispersal agents, phylogenetic trees were well resolved and highly consistent across both data sets and all methods. We inferred that the most likely root, based on marginal likelihood comparisons, is to the east and south of the region of highest genetic diversity, which lies along the coast of the Gulf of California in Sonora, Mexico. Together with striking decreases in marginal likelihood found to the north, this supports hypotheses that saguaro’s current range reflects post-glacial expansion from the refugia in the south of its range. We conclude with observations about practical and theoretical issues raised by phylogenomic data sets within species, in which SNP-based methods must be used rather than gene tree methods that are widely used when sequence divergence is higher. These include computational scalability, inference of gene flow, and proper assessment of statistical support in the presence of linkage effects.

Are 150 km of open sea enough? Gene flow and population differentiation in a bat-pollinated columnar cactus

“…Thus, it is likely that populations showing high genetic diversities such as Zacate Blanco and Nopolo retain the ancestral haplotypes and were Pleistocene refuges. A similar pattern was found by Sanderson et al [ 75 ] for saguaro. Expanding studies to other populations and using information from the whole-genome throughout the species’ natural range should be of interest (particularly those on islands) and reveal adaptive differentiation among populations [ 4 , 76 ].…”

Are 150 km of open sea enough? Gene flow and population differentiation in a bat-pollinated columnar cactus

“…We did not find higher levels of genetic diversity in what were the likely Pleistocene refuges as found by Sanderson et al [79] for saguaro with many more markers.…”

“…Still, evidence of local adaptation needs to be assessed and the intensity and direction of selection quantified, requiring comparison with phenotypic traits and assessment of survival over time [78]. We did not find higher levels of genetic diversity in what were the likely Pleistocene refuges as found by Sanderson et al [79] for saguaro with many more markers. Expanding studies to other populations and using information from the whole-genome throughout the species’ natural range should be of interest (particularly those on islands) and reveal adaptive differentiation among populations [4, 80].…”

An improved genome assembly of the saguaro cactus (Carnegiea gigantea(Engelm.) Britton & Rose)

“…However, limited financial availability and difficulty in sample preparation still prevent the genomes of certain organisms from being fully characterized. Despite being an extreme example of physiological and morphological adaptation, until recently little or no genomic resources were available for cactus species [1][2][3][4] .…”