Population genomics of divergence within an obligate pollination mutualism: Selection maintains differences between Joshua tree species.
OBJECTIVE
Speciation is a complex process that can be shaped by many factors, from geographic isolation to interspecific interactions. In Joshua trees, selection from pollinators on style length has been hypothesized to contribute to the maintenance of differentiation between two hybridizing sister species. We used population genomics approaches to measure the extent of genetic differentiation between these species, test whether selection maintains differences between them, and determine whether genetic variants associated with style length show signatures of selection.


METHODS
Using restriction-site-associated DNA (RAD)-sequencing, we identified 9516 single nucleotide polymorphisms (SNPs) across the Joshua tree genome. We characterized the genomic composition of trees in a narrow hybrid zone and used genomic scans to search for signatures of selection acting on these SNPs. We used a genome-wide association study to identify SNPs associated with variation in phenotypic traits, including style length, and asked whether those SNPs were overrepresented among the group under selection.


RESULTS
The two species were highly genetically differentiated (FST= 0.25), and hybrids were relatively rare in the hybrid zone. Approximately 20% of SNPs showed evidence of selection maintaining divergence. While SNPs associated with style length were overrepresented among those under selection (P << 0.0001), the same was true for SNPs associated with highly differentiated vegetative traits.


CONCLUSIONS
The two species of Joshua tree are clearly genetically distinct, and selection is maintaining differences between them. We found that loci associated with differentiated traits were likely to be under selection. However, many traits other than style length appeared to be under selection. Together with the dearth of intermediate hybrids, these findings reveal that these taxa are more strongly diverged than previously suspected and that selection, likely on many targets, is maintaining separation where the two species meet and hybridize.
Department of Biology, Willamette University, Salem, Oregon 97301 USA aroyer@willamette.edu.
Anne M
AM
Royer
Institute of Ecology and Evolution, University of Oregon, Eugene, Oregon 97403 USA.
Matthew A
MA
Streisfeld
Department of Biology, Willamette University, Salem, Oregon 97301 USA.
Christopher Irwin
CI
Smith
D000818:Animals; D018745:Genome, Plant; D055106:Genome-Wide Association Study; D056186:Metagenomics; D009036:Moths / Q000502:physiology*; D009505:Nevada; D054817:Pollination; D020641:Polymorphism, Single Nucleotide; D012641:Selection, Genetic; D017422:Sequence Analysis, DNA; D013045:Species Specificity; D013559:Symbiosis; D027623:Yucca / Q000235:genetics / Q000502:physiology*
Asparagaceae; RAD-sequencing; Tegeticula; Yucca brevifolia; Yucca jaegeriana; disruptive selection; divergent selection; hybridization; mutualism