Phylogenomic Studies of Character Evolution in Neo-Astragalus (Astragalus L., Fabaceae)

Abstract

The evolution of species radiations has involved two processes: diversification, or the formation of many species, as well as disparification, the differentiation of species in traits associated with differing ecological niches. Extremes of disparification are a hallmark of classic examples of adaptive radiations, which have also often proceeded with comparable rates of diversification. While disparification is thought to be limited in nonadaptive radiations, the focus of studies on large groups of grossly ecologically similar species has often been on rates of diversification rather than on levels of ecological and associated morphological or physiological differentiation. Disparification in nonadaptive radiations may very well have occurred but involved cryptic or difficult to observe, yet ecologically important traits. Disparity in cryptic traits may also involve convergent evolution or homoplasy, which may be difficult to document without well-resolved phylogenies that have often remained elusive in large groups of recently radiated species. The radiation of the Neo-Astragalus clade of Astragalus L. (Fabaceae), a group of nearly 500 species of largely temperate, perennial herbaceous plants in North and South America, is estimated to have occurred only in the last ca. 4.4 Ma. I estimate greatly improved phylogenies of Neo-Astragalus to examine the evolution of multiple types of characters and shed light on cryptic differentiation and homoplasy within this large clade. While not as disparate in climatic niche or growth form as classic examples of plant adaptive radiations, Neo-Astragalus species do display key differences in cryptic but ecologically important traits such as specialization on specific geological substrates and the production of different kinds of toxins, as well as in morphological characters (especially of the fruit) and characters of genomic organization. In Chapter 1, I examine the structure of Neo-Astragalus plastomes with regard to the abundance and placement of repeated sequences and the locations of endpoints of large inversions found in several Neo-Astragalus species. Specific repeated sequences near inversion endpoints shed light on the potential mechanisms of inversion formation and retention and also reveal inversions in two species with endpoints between the same sets of loci to be homoplastic. In Chapter 2, I estimate improved phylogenies of Neo-Astragalus from a broad taxonomic sampling of species using both plastome and nuclear ribosomal DNA (nrDNA) sequences. These phylogenies resolve relationships within Neo-Astragalus to a much greater extent than ever before but also reveal rampant homoplasy in morphological characters used to form the taxonomic system of <i>Astragalus</i> in North America. In Chapter 3, I characterize the trait of selenium hyperaccumulation with chemical assays of individuals from 26 Neo-Astragalus species either previously documented as or assumed to be accumulators of the element. Reconstructing the evolutionary history of this trait reveals there were multiple independent origins of selenium hyperaccumulation in the Neo-Astragalus clade, although the exact number and placement of these origins are less certain. Homoplasy, which I document in plastome inversions, morphological characters, and through multiple independent origins of selenium hyperaccumulation, is a striking feature of character evolution in Neo-Astragalus. This homoplasy, especially in selenium hyperaccumulation, may be indicative of even greater disparification that accompanied the evolution of Neo-Astragalus in cryptic but ecologically relevant traits, including substrate specialization and the production of toxic compounds.