The Ascent of the Abundant: How Mutational Networks Constrain Evolution

Evolution by natural selection is fundamentally shaped by the fitness landscapes in which it occurs. Yet fitness landscapes are vast and complex, and thus we know relatively little about the long-range constraints they impose on evolutionary dynamics. Here, we exhaustively survey the structural landscapes of RNA molecules of lengths 12 to 18 nucleotides, and develop a network model to describe the relationship between sequence and structure. We find that phenotype abundance—the number of genotypes producing a particular phenotype—varies in a predictable manner and critically influences evolutionary dynamics. A study of naturally occurring functional RNA molecules using a new structural statistic suggests that these molecules are biased toward abundant phenotypes. This supports an “ascent of the abundant” hypothesis, in which evolution yields abundant phenotypes even when they are not the most fit

The global distribution of known and undiscovered ant biodiversity

Invertebrates constitute the majority of animal species and are critical for ecosystem functioning and services. Nonetheless, global invertebrate biodiversity patterns and their congruences with vertebrates remain largely unknown. We resolve the first high-resolution (~20-km) global diversity map for a major invertebrate clade, ants, using biodiversity informatics, range modeling, and machine learning to synthesize existing knowledge and predict the distribution of undiscovered diversity. We find that ants and different vertebrate groups have distinct features in their patterns of richness and rarity, underscoring the need to consider a diversity of taxa in conservation. However, despite their phylogenetic and physiological divergence, ant distributions are not highly anomalous relative to variation among vertebrate clades. Furthermore, our models predict that rarity centers largely overlap (78%), suggesting that general forces shape endemism patterns across taxa. This raises confidence that conservation of areas important for small-ranged vertebrates will benefit invertebrates while providing a “treasure map” to guide future discovery.The Okinawa Institute of Science and Technology Graduate University, the Japan Society for the Promotion of Science, Japan Society for the Promotion of Science Postdoctoral Fellowships for Foreign Researchers Program, Japan Ministry of the Environment, Environment Research, and Technology Development Fund no. 4-1904, the Leverhulme Trust, the National Science Foundation, Australian Research Discovery Grant, Foundational Biodiversity Information Programme (South Africa), and the USDA and NIFA support of the Mississippi Entomological Museum.https://www.science.org/journal/sciadvam2023Zoology and Entomolog

The origins, maintenance, and conservation of biodiversity in spatial networks

textBiodiversity is distributed unevenly across geographic space and the tree of life. A key task of biology is to understand the ecological and evolutionary processes that generate these patterns. I investigate how the structure and geometry of a landscape, for example the sizes and arrangements of islands in an archipelago, affects processes contributing to the generation and conservation of biodiversity patterns. In the first chapter, I integrate two disparate bodies of theory, ecological neutral theory and network theory into a powerful new framework for investigating patterns of biodiversity in a complex landscape. I examine the consequences of network structure, such as size, topology, and connectivity, for diversity patterning across the metacommunity. The second chapter focuses on how the position of a node within a network controls local community (node) diversity. Network statistics, such as node centrality, are found to predict diversity patterns with more central nodes accumulating the most diversity. In the third chapter, I use the theory to evaluate how well fundamental concepts in conservation biology perform when neutral metacommunity processes generate diversity patterns. I find that contemporary diversity patterns are poor predictors of the long-term capacity of a network to support diversity, challenging a host of conservation concepts and applications. In the fourth chapter, I consider biodiversity dynamics in a network with a different model of speciation, where spatial structure is needed for divergence. In this case, speciation hotspots form where the dispersal properties of an organism and the spatial structure of the landscape coincide. In the final chapter I study the biodiversity of a natural structured metacommunity, the ants of the Fijian archipelago. I used a variety of collecting techniques to inventory the ant species occurring across a system of islands in the southwest Pacific. Approximately 50 new species were discovered, and the distributions of the ant species across the islands are firmly established. Radiations are observed in the genera Pheidole, Camponotus, Lordomyrma, Leptogenys, Cerapachys, Strumigenys, Poecilomyrma, and Hypoponera.Ecology, Evolution and Behavio

Sequencing degraded DNA from non-destructively sampled museum specimens for RAD-tagging and low-coverage shotgun phylogenetics.

Ancient and archival DNA samples are valuable resources for the study of diverse historical processes. In particular, museum specimens provide access to biotas distant in time and space, and can provide insights into ecological and evolutionary changes over time. However, archival specimens are difficult to handle; they are often fragile and irreplaceable, and typically contain only short segments of denatured DNA. Here we present a set of tools for processing such samples for state-of-the-art genetic analysis. First, we report a protocol for minimally destructive DNA extraction of insect museum specimens, which produced sequenceable DNA from all of the samples assayed. The 11 specimens analyzed had fragmented DNA, rarely exceeding 100 bp in length, and could not be amplified by conventional PCR targeting the mitochondrial cytochrome oxidase I gene. Our approach made these samples amenable to analysis with commonly used next-generation sequencing-based molecular analytic tools, including RAD-tagging and shotgun genome re-sequencing. First, we used museum ant specimens from three species, each with its own reference genome, for RAD-tag mapping. Were able to use the degraded DNA sequences, which were sequenced in full, to identify duplicate reads and filter them prior to base calling. Second, we re-sequenced six Hawaiian Drosophila species, with millions of years of divergence, but with only a single available reference genome. Despite a shallow coverage of 0.37 ± 0.42 per base, we could recover a sufficient number of overlapping SNPs to fully resolve the species tree, which was consistent with earlier karyotypic studies, and previous molecular studies, at least in the regions of the tree that these studies could resolve. Although developed for use with degraded DNA, all of these techniques are readily applicable to more recent tissue, and are suitable for liquid handling automation

RAD-tag reads mapped to reference ant genomes

The archive contains 6 BAM files with genomic reads from three species of ants mapped to their respective reference genomes

Genomic reads of 6 Hawaiian Drosophila species mapped to the D. grimshawi genome

File is in standard BAM format. Species names are identified by read groups IDs

Specimens used in this study, and DNA yields.

<p>See <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0096793#pone-0096793-g002" target="_blank">Figure 2</a> for data on the fragment size distribution in the libraries. The number of reads is much higher for the <i>Drosophila</i> libraries because they were sequenced exhaustively on a HiSeq, as well as a MiSeq platform.</p

Schematic overview of the library preparation process.

<p>Both RAD-tag (left) and whole-genome shotgun (right) library preparation methods start the same way, and diverge only at the final stage. (a) DNA is heated to denature the template strands. (b) Terminal deoxynucleotidyl transferase (TdT) is used to add a riboguanidine tail of a determined length <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0096793#pone.0096793-Schmidt1" target="_blank">[44]</a>. (c) Priming with the Illumina P2 adaptor sequence, the Klenow exo- fragment generates the second strand. At this point, T4 DNA polymerase treatment is necessary to blunt the DNA fragments. After (d’) for RAD-tag sequencing, EcoRI is used to digest a subset of the fragments. (d’’ and e) a final ligation step adds the P1 Illumina adaptor sequence. Barcodes are ligated in-line, upstream of the read one sequencing primer binding site. After ligation of the final adaptor sequence, fragments are PCR-amplified to complete the sequencing adaptor. All libraries contained in-line barcodes in front of the read one sequencing site.</p

Fragment sizes of extracted DNA for ants (A) and fruit flies (B).

<p>Virtually all fragments in the libraries were less than 100-axis are derived from Bioanalyzer traces, and are somewhat arbitrary, giving only an approximate indication of extraction yield. See <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0096793#pone-0096793-t001" target="_blank">Table 1</a> for more details on the actual yield from each extraction. We failed to amplify an approximately 700-bp fragment of mitochondrial DNA from these specimens using a popular primer set <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0096793#pone.0096793-Folmer1" target="_blank">[22]</a>.</p

The global distribution of known and undiscovered ant biodiversity

Invertebrates constitute the majority of animal species and are critical for ecosystem functioning and services. Nonetheless, global invertebrate biodiversity patterns and their congruences with vertebrates remain largely unknown. We resolve the first high-resolution (~20-km) global diversity map for a major invertebrate clade, ants, using biodiversity informatics, range modeling, and machine learning to synthesize existing knowledge and predict the distribution of undiscovered diversity. We find that ants and different vertebrate groups have distinct features in their patterns of richness and rarity, underscoring the need to consider a diversity of taxa in conservation. However, despite their phylogenetic and physiological divergence, ant distributions are not highly anomalous relative to variation among vertebrate clades. Furthermore, our models predict that rarity centers largely overlap (78%), suggesting that general forces shape endemism patterns across taxa. This raises confidence that conservation of areas important for small-ranged vertebrates will benefit invertebrates while providing a "treasure map" to guide future discovery