Radiation of the rock daisies in the desert mountains of the southwest U.S. and northern Mexico: a phylogenomic, systematic, and historical biogeographic analysis of tribe Perityleae (Compositae)

Rock daisies (Perityleae; Compositae) are a diverse clade of seven genera and ca. 84 minimum-rank taxa that mostly occur as narrow endemics on sheer rock-cliffs throughout the southwest U.S. and northern Mexico. Taxonomy of Perityleae has traditionally been based on morphology and cytogenetics. To test taxonomic hypotheses and utility of characters emphasized in past treatments, we present the first densely sampled molecular phylogenies of Perityleae and reconstruct trait and chromosome evolution. We inferred phylogenetic trees from whole chloroplast genomes, nuclear ribosomal cistrons, and hundreds of low-copy nuclear genes using genome skimming and target-capture. Discordance between sources of molecular data suggests an underappreciated history of hybridization in Perityleae. Phylogenies support the monophyly of subtribe Peritylinae, a distinctive group possessing a four-lobed disc corolla; however, all the phylogenetic trees generated in this study reject the monophyly of the most species-rich genus, Perityle, as well as its sections: Perityle sect. Perityle, Perityle sect. Laphamia, and Perityle sect. Pappothrix. Results of reversible jump MCMC suggest that morphological characters traditionally used to classify members of Perityleae have evolved multiple times within the group. A base chromosome number of x=9 gave rise to higher base numbers in subtribe Peritylinae (x=12, 13, 16, 17, 18 and 19) through polyploidization followed by ascending or descending dysploidy. Most taxa constitute a monophyletic lineage with a base chromosome number of x=17, with multiple neo-polyploidization events. These results demonstrate the advantages and obstacles to next-generation sequencing approaches in synantherology while laying the foundation for taxonomic revision and comparative study of the evolutionary ecology of Perityleae./nPhylogenomic analyses of sequence data from chloroplast and nuclear genomes as well as morphological and cytological analyses resolves long standing phylogenetic uncertainty in the rock daisy tribe (Perityleae; Asteraceae) and supports reclassification at the generic level to reflect evolutionary relationships. The previously recognized genera Eutetras, Amauria, and Pericome were all upheld as clades and continue to be recognized in the new classification. The large genus Perityle as treated in previous taxonomies was found not to be monophyletic and is thus reclassified in four genera, using the available names Laphamia (in an expanded sense), Galinsogeopsis (in an expanded sense), Nesothamnus, and Perityle (in a restricted sense). The type species of Perityle belongs to an early diverging lineage of the rock daisy tribe, in a clade including four other minimum-rank taxa of northwest Mexican annuals, with base chromosome numbers of x=11, 12, 13, 16, or 19. Nesothamnus is reinstated as a monotypic genus for the Guadalupe island endemic shrub Nesothamnus incanus. Laphamia and Galinsogeopsis together constitute a clade of woody and herbaceous perennials or annuals with a stabilized base chromosome number of x=17 (n=34, 51, 68) that have diversified throughout the Basin and Range Province and the Sierra Madre Occidental of the southwest U.S. and northern Mexico. Laphamia and Galinsogeopsis have overlapping geographic distributions but can be distinguished by a combination of fruit and flower traits. This new generic classification of Perityleae resolves long standing conflict about the circumscription of Perityle without expanding the genus to encompass the entire subtribe Peritylinae and recognizes two independent evolutionary radiations onto island-like rock habitats in the North American deserts as taxonomically distinct components of this fascinating tribe of composites./nEvolutionary diversifications in extreme environments like islands, mountain tops, and deserts stand out as some of the most unexpected achievements of life on earth. These evolutionary radiations have taken place in recently emerged, novel ecosystems and therefore challenge prevailing ideas about niche conservatism, but in general, we know little about the conditions that precipitate successful shifts into novel biomes and lead to diversification there. Here, we investigate the roles of adaptive evolution and pre-adaptation during shifts into the North American Deserts in the rock daisies (Perityleae). We sequenced 74 additional samples of Perityleae from across two geographically separated regions of biome contact between tropical deciduous forests and deserts in the Baja California peninsula and northwest mainland Mexico. We infer the first densely sampled time-calibrated phylogenetic hypothesis for this tribe based on a target capture sequence dataset and reconstruct their historical biogeography and ecology using Bayesian statistical inference with paleobiome-informed models, finding evidence for seven independent shifts into desert habitats occurring since the onset of aridification in the mid-Miocene. The earliest of these shifts occurred in the late Miocene out of tropical deciduous forests in northwest Mexico and led to an extensive radiation throughout all the North American deserts of species in the genus Laphamia, which account for the majority of extant desert Perityleae. Through detailed reconstructions of life-history and micro-habitat, we find evidence for a tight evolutionary correlation between a suffrutescent life history strategy and strict edaphic affinities for bare rocky outcrops in Perityleae, making it possible to infer historical occupancy of bare habitats as a precursor to successful shifts into the desert biome. Our analysis shows that the extensive diversification of desert Perityleae in the genus Laphamia descended from ancestors pre-adapted for dry conditions through past ecological specialization onto edaphically arid rock outcrops in the otherwise densely vegetated tropical deciduous forests of northwest Mexico. This provides some of the first empirical support for the long-standing hypothesis that desert plants evolved unique life forms prior to the onset of widespread arid conditions through pre-adaptation to edaphically dry microsites within older biomes, enabling them to readily shift and diversify in the novel environments as they recently emerged.

Advisor: Baldwin, Bruce G