Plastid genome evolution in leafless members of the orchid subfamily Orchidoideae, with a focus on Degranvillea dermaptera.

PREMISE: Leafless, heterotrophic plants are prime examples of organismal modification, the genomic consequences of which have received considerable interest. In particular, plastid genomes (plastomes) are being sequenced at a high rate, allowing continual refinement of conceptual models of reductive evolution in heterotrophs. However, numerous sampling gaps exist, hindering the ability to conduct comprehensive phylogenomic analyses in these plants. METHODS: Using floral tissue from an herbarium specimen, we sequenced and analyzed the plastome of Degranvillea dermaptera, a rarely collected, leafless orchid species from South America about which little is known, including its phylogenetic affinities. RESULTS: The plastome is the most reduced of those sequenced among the orchid subfamily Orchidoideae. In Degranvillea, it has lost the majority of genes found in leafy autotrophic species, is structurally rearranged, and has similar gene content to the most reduced plastomes among the orchids. We found strong evidence for the placement of Degranvillea within the subtribe Spiranthinae using models that explicitly account for heterotachy, or lineage-specific evolutionary rate variation over time. We further found evidence of relaxed selection on several genes and of correlations among substitution rates and several other "traits" of the plastome among leafless members of orchid subfamily Orchidoideae. CONCLUSIONS: Our findings advance knowledge on the phylogenetic relationships and paths of plastid genome evolution among the orchids, which have experienced more independent transitions to heterotrophy than any other plant family. This study demonstrates the importance of herbarium collections in comparative genomics of poorly known species of conservation concern.

Organellar phylogenomics at the epidendroid orchid base, with a focus on the mycoheterotrophic Wullschlaegelia.

BACKGROUND AND AIMS: Heterotrophic plants have long been a challenge for systematists, exemplified by the base of the orchid subfamily Epidendroideae, which contains numerous mycoheterotrophic species. METHODS: Here we address the utility of organellar genomes in resolving relationships at the epidendroid base, specifically employing models of heterotachy, or lineage-specific rate variation over time. We further conduct comparative analyses of plastid genome evolution in heterotrophs and structural variation in matK. KEY RESULTS: We present the first complete plastid genomes (plastomes) of Wullschlaegelia, the sole genus of the tribe Wullschlaegelieae, revealing a highly reduced genome of 37 kilobases, which retains a fraction of the genes present in related autotrophs. Plastid phylogenomic analyses recovered a strongly supported clade composed exclusively of mycoheterotrophic species with long branches. We further analyzed mitochondrial gene sets, which recovered similar relationships to those in other studies using nuclear data, but the placement of Wullschlaegelia remains uncertain. We conducted comparative plastome analyses among Wullschlaegelia and other heterotrophic orchids, revealing a suite of correlated substitutional and structural changes relative to autotrophic species. Lastly, we investigated evolutionary and structural variation in matK, which is retained in Wullschlaegelia and a few other 'late stage' heterotrophs and found evidence for structural conservation despite rapid substitution rates in both Wullschlaegelia and the leafless Gastrodia. CONCLUSIONS: Our analyses reveal the limits of what the plastid genome can tell us on orchid relationships in this part of the tree, even when applying parameter-rich heterotachy models. Our study underscores the need for increased taxon sampling across all three genomes at the epidendroid base, and illustrates the need for further research on addressing heterotachy in phylogenomic analyses.

Independent origins of Spiranthes×kapnosperia (Orchidaceae) and their nomenclatural implications.

Spiranthes Rich. (Orchidaceae) is a commonly encountered but systematically and nomenclaturally challenging component of the North American orchid flora. Here, the evolutionary history and hybrid origin of the recently described S.sheviakii Hough and Young are critically examined. The available molecular data unambiguously support a hybrid origin of S.cernua (L.) Rich. × S.ochroleuca (Rydb.) Rydb. for S.sheviakii, the same parentage as the priority name S.×kapnosperia M.C. Pace. As hybrid formulas can have only one correct name, S.sheviakii is a synonym of S.×kapnosperia. It is likely that S.×kapnosperia evolved independently at least twice in at least two widely disjunct locations.

Spatial phylogenetics reveals evolutionary constraints on the assembly of a large regional flora.

PREMISE OF THE STUDY: We used spatial phylogenetics to analyze the assembly of the Wisconsin flora, linking processes of dispersal and niche evolution to spatial patterns of floristic and phylogenetic diversity and testing whether phylogenetic niche conservatism can account for these patterns. METHODS: We used digitized records and a new molecular phylogeny for 93% of vascular plants in Wisconsin to estimate spatial variation in species richness and phylogenetic α and ß diversity in a native flora shaped mainly by postglacial dispersal and response to environmental gradients. We developed distribution models for all species and used these to infer fine-scale variation in potential diversity, phylogenetic distance, and interspecific range overlaps. We identified 11 bioregions based on floristic composition, mapped areas of neo- and paleo-endemism to establish new conservation priorities and predict how community-assembly patterns should shift with climatic change. KEY RESULTS: Spatial phylogenetic turnover most strongly reflects differences in temperature and spatial distance. For all vascular plants, assemblages shift from phylogenetically clustered to overdispersed northward, contrary to most other studies. This pattern is lost for angiosperms alone, illustrating the importance of phylogenetic scale. CONCLUSIONS: Species ranges and assemblage composition appear driven primarily by phylogenetic niche conservatism. Closely related species are ecologically similar and occupy similar territories. The average level and geographic structure of plant phylogenetic diversity within Wisconsin are expected to greatly decline over the next half century, while potential species richness will increase throughout the state. Our methods can be applied to allochthonous communities throughout the world.

Evolution of geographical place and niche space: Patterns of diversification in the North American sedge (Cyperaceae) flora.

The role of geography and ecology in speciation are often discussed in the context of phylogenetic niche conservatism (PNC), the propensity of lineages to retain ancestral niche related traits. However, a recent paradigm shift focuses instead on measuring divergence of these traits in conjunction with patterns of speciation. Under this framework, we analyzed the diversification of North America's third most diverse family, Cyperaceae ("sedges"), using a modified Parsimony Analysis of Endemicity approach to identify floristic regions and ordination statistics to quantify species distribution in a continuous manner. Utilizing over 200,000 georeferenced specimens, we characterized the geographical distribution and climatic and edaphic niche space occupied by each species. We constructed a supermatrix phylogeny of the North American sedge flora, aided in part by the sequencing of all sedges of Wisconsin, and employed a multifaceted approach to assess the role of geographical and ecological divergence on lineage diversification. In addition to measuring phylogenetic signal for these traits, we also measured pairwise phylogenetic distance of species within floristic regions, calculated rates of speciation, and tested for correlations of speciation rate to tempo of geographical and ecological evolution. Our analyses consistently show that evolutionarily related species tend to be geographically unrelated. Rates of geographical and ecological diversification are closely linked to tempo of speciation, and exploration of geographical place coincides with divergence in ecological niche space. We highlight the benefits of treating geography in a continuous manner, and stress the importance of employing a diverse suite of analytical approaches in testing hypotheses regarding the evolution of range and niche.