Clayton J. Visger

Polyploidy and novelty: Gottlieb's legacy

Nearly four decades ago, Roose & Gottlieb (Roose & Gottlieb 1976 Evolution 30, 818–830. (doi:10.2307/2407821)) showed that the recently derived allotetraploids Tragopogon mirus and T. miscellus combined the allozyme profiles of their diploid parents (T. dubius and T. porrifolius, and T. dubius and T. pratensis, respectively). This classic paper addressed the link between genotype and biochemical phenotype and documented enzyme additivity in allopolyploids. Perhaps more important than their model of additivity, however, was their demonstration of novelty at the biochemical level. Enzyme multiplicity—the production of novel enzyme forms in the allopolyploids—can provide an extensive array of polymorphism for a polyploid individual and may explain, for example, the expanded ranges of polyploids relative to their diploid progenitors. In this paper, we extend the concept of evolutionary novelty in allopolyploids to a range of genetic and ecological features. We observe that the dynamic nature of polyploid genomes—with alterations in gene content, gene number, gene arrangement, gene expression and transposon activity—may generate sufficient novelty that every individual in a polyploid population or species may be unique. Whereas certain combinations of these features will undoubtedly be maladaptive, some unique combinations of newly generated variation may provide tremendous evolutionary potential and adaptive capabilities.

Polyploidy: Pitfalls and paths to a paradigm

Investigators have long searched for a polyploidy paradigm-rules or principles that might be common following polyploidization (whole-genome duplication, WGD). Here we attempt to integrate what is known across the more thoroughly investigated polyploid systems on topics ranging from genetics to ecology. We found that while certain rules may govern gene retention and loss, systems vary in the prevalence of gene silencing vs. homeolog loss, chromosomal change, the presence of a dominant genome (in allopolyploids), and the relative importance of hybridization vs. genome doubling per se. In some lineages, aspects of polyploidization are repeated across multiple origins, but in other species multiple origins behave more stochastically in terms of genetic and phenotypic change. Our investigation also reveals that the path to synthesis is hindered by numerous gaps in our knowledge of even the best-known systems. Particularly concerning is the absence of linkage between genotype and phenotype. Moreover, most recent studies have focused on the genetic and genomic attributes of polyploidy, but rarely is there an ecological or physiological context. To promote a path to a polyploidy paradigm (or paradigms), we propose a major community goal over the next 10-20 yr to fill the gaps in our knowledge of well-studied polyploids. Before a meaningful synthesis is possible, more complete data sets are needed for comparison-systems that include comparable genetic, genomic, chromosomal, proteomic, as well as morphological, physiological, and ecological data. Also needed are more natural evolutionary model systems, as most of what we know about polyploidy continues to come from a few crop and genetic models, systems that often lack the ecological context inherent in natural systems and necessary for understanding the drivers of biodiversity.

An Exploration into Fern Genome Space

Ferns are one of the few remaining major clades of land plants for which a complete genome sequence is lacking. Knowledge of genome space in ferns will enable broad-scale comparative analyses of land plant genes and genomes, provide insights into genome evolution across green plants, and shed light on genetic and genomic features that characterize ferns, such as their high chromosome numbers and large genome sizes. As part of an initial exploration into fern genome space, we used a whole genome shotgun sequencing approach to obtain low-density coverage (∼0.4X to 2X) for six fern species from the Polypodiales (Ceratopteris, Pteridium, Polypodium, Cystopteris), Cyatheales (Plagiogyria), and Gleicheniales (Dipteris). We explore these data to characterize the proportion of the nuclear genome represented by repetitive sequences (including DNA transposons, retrotransposons, ribosomal DNA, and simple repeats) and protein-coding genes, and to extract chloroplast and mitochondrial genome sequences. Such initial sweeps of fern genomes can provide information useful for selecting a promising candidate fern species for whole genome sequencing. We also describe variation of genomic traits across our sample and highlight some differences and similarities in repeat structure between ferns and seed plants.

A global perspective on Campanulaceae: Biogeographic, genomic, and floral evolution

PREMISE OF THE STUDY The Campanulaceae are a diverse clade of flowering plants encompassing more than 2300 species in myriad habitats from tropical rainforests to arctic tundra. A robust, multigene phylogeny, including all major lineages, is presented to provide a broad, evolutionary perspective of this cosmopolitan clade. METHODS We used a phylogenetic framework, in combination with divergence dating, ancestral range estimation, chromosome modeling, and morphological character reconstruction analyses to infer phylogenetic placement and timing of major biogeographic, genomic, and morphological changes in the history of the group and provide insights into the diversification of this clade across six continents. KEY RESULTS Ancestral range estimation supports an out-of-Africa diversification following the Cretaceous-Tertiary extinction event. Chromosomal modeling, with corroboration from the distribution of synonymous substitutions among gene duplicates, provides evidence for as many as 20 genome-wide duplication events before large radiations. Morphological reconstructions support the hypothesis that switches in floral symmetry and anther dehiscence were important in the evolution of secondary pollen presentation mechanisms. CONCLUSIONS This study provides a broad, phylogenetic perspective on the evolution of the Campanulaceae clade. The remarkable habitat diversity and cosmopolitan distribution of this lineage appears to be the result of a complex history of genome duplications and numerous long-distance dispersal events. We failed to find evidence for an ancestral polyploidy event for this clade, and our analyses indicate an ancestral base number of nine for the group. This study will serve as a framework for future studies in diverse areas of research in Campanulaceae.

Evolution and biogeography of the endemic Roucela complex (Campanulaceae: Campanula) in the Eastern Mediterranean

Abstract At the intersection of geological activity, climatic fluctuations, and human pressure, the Mediterranean Basin – a hotspot of biodiversity – provides an ideal setting for studying endemism, evolution, and biogeography. Here, we focus on the Roucela complex (Campanula subgenus Roucela), a group of 13 bellflower species found primarily in the eastern Mediterranean Basin. Plastid and low‐copy nuclear markers were employed to reconstruct evolutionary relationships and estimate divergence times within the Roucela complex using both concatenation and species tree analyses. Niche modeling, ancestral range estimation, and diversification analyses were conducted to provide further insights into patterns of endemism and diversification through time. Diversification of the Roucela clade appears to have been primarily the result of vicariance driven by the breakup of an ancient landmass. We found geologic events such as the formation of the mid‐Aegean trench and the Messinian Salinity Crisis to be historically important in the evolutionary history of this group. Contrary to numerous past studies, the onset of the Mediterranean climate has not promoted diversification in the Roucela complex and, in fact, may be negatively affecting these species. This study highlights the diversity and complexity of historical processes driving plant evolution in the Mediterranean Basin.

Population genetic variation, geographic structure, and multiple origins of autopolyploidy in Galax urceolata

PREMISE OF THE STUDY Whereas population genetic studies have examined allopolyploids, comparable studies of naturally occurring autopolyploids remain rare. To address fundamental questions regarding autopolyploidy, we undertook a detailed population genetic study of one of the classic examples of autopolyploidy, Galax urceolata (Diapensiaceae), which comprises diploid, triploid, and autotetraploid cytotypes. Galax is endemic to the Appalachian Mountains, the adjacent piedmont, sandhills, and coastal plain and represents perhaps the most widely known example of autopolyploidy in nature. METHODS Flow cytometry was used to diagnose ploidal level of ∼1000 individuals across 71 populations. We used 10 microsatellite markers to examine genetic variation across the geographic range of Galax and assessed multiple origins though comparisons of diploid, triploid, and tetraploid accessions using multiple analytical approaches. KEY RESULTS Tetraploids had higher levels of heterozygosity than diploids did. Genetic variation in diploid and tetraploid Galax is geographically structured among the ecoregions of the southeastern United States. Autotetraploidy in Galax urceolata has occurred independently at least 46 times, with triploidy having occurred a minimum of 31 times. CONCLUSIONS Genetic differentiation among ecoregions suggests historical patterns of local adaptation. The numerous independent origins of tetraploid Galax reported here are among the highest frequencies of independent polyploidizations ever reported for any polyploid (auto- or allopolyploid).

Niche divergence between diploid and autotetraploid Tolmiea

PREMISE OF STUDY Polyploidy is common in eukaryotes and is of major evolutionary importance over both short and long time-scales. Compared to allopolyploids, autopolyploids remain understudied; they are often morphologically cryptic and frequently remain taxonomically unrecognized, although there is increasing recognition of the high frequency of autopolyploidy in angiosperms. While autopolyploidy can serve as an instant speciation mechanism, little is known about the ecological consequences of this process. We describe the ecological divergence of a diploid-autotetraploid species pair in Tolmiea. METHODS We investigated whether abiotic niche divergence has shaped the current allopatric distribution of diploid T. diplomenziesii and its autotetraploid derivative, T. menziesii, in the Pacific Northwest of North America. We employed field measures of light availability, as well as niche modeling and a principal component analysis of environmental space. Within a common garden, we also investigated physiological responses to changes in soil moisture. KEY RESULTS Diploid and autotetraploid Tolmiea inhabit significantly different climatic niche spaces. The climatic niche divergence between these two species is best explained by a shift in precipitation availability, and we found evidence of differing physiological response to water availability between these species. CONCLUSIONS We found that spatial segregation of T. diplomenziesii and T. menziesii was accompanied by adaptation to changes in climatic regime. Tolmiea menziesii is not a nascent autotetraploid, having persisted long enough to be established throughout the Pacific Northwest, and therefore both polyploidization and subsequent evolution have contributed to the observed differences between T. menziesii and T. diplomenziesii.

Origins and diversity of a cosmopolitan fern genus on an island archipelago

Isolated oceanic islands are characterized by patterns of biological diversity different from those on continents. Nucleotide sequences from chloroplast and nuclear genes were used to examine the origins and diversity of the cosmopolitan fern genus Pteridium on the Galapagos Islands. We found evidence for multiple origins of the widespread allotetraploid P. caudatum. We also show that the Galapagos Islands are home to P. caudatum as well as diploid P. esculentum subsp. arachnoideum and possible hybrids between the two. Haplotype diversity indicates that Pteridium has colonized the islands multiple times and probably from diverse mainland sources.

Geographic Range Dynamics Drove Ancient Hybridization in a Lineage of Angiosperms

Elucidating the dynamic distribution of organismal lineages has been central to biology since the nineteenth century, yet the difficulty of combining biogeographic methods with shifts in habitat suitability remains a limitation. This integration, however, is critical to understanding geographic distributions, present and past, as well as the time-extended trajectories of lineages. Here, we link previous advances in phyloclimatic modeling to develop a framework that overcomes existing methodological gaps by predicting potential ecological and geographic overlap directly from estimated ancestral trait distributions. We show the utility of this framework by focusing on a clade in the montane angiosperm genus Heuchera, which is noteworthy in that it experienced ancient introgression from circumboreally distributed species of Mitella, lineages now ~1,300 km disjunct. Using this system, we demonstrate an application of ancestral state reconstruction to assess geographic range dynamics in a lineage lacking a fossil record. We test hypotheses regarding inferred past geographic distributions and examine the potential for ancient geographic contact. Application of this multifaceted approach suggests potential past contact between species of Heuchera and Mitella in western North America during cooler periods of the Pleistocene. Integration of niche models and phylogenetic estimates suggests that climatic cooling may have promoted range contact and gene flow between currently highly disjunct species. Our approach has wide applicability for testing hypotheses concerning organismal co-occurrences in deep time.