jocelyn colella

Connecting next-generation museum collections to public health

Marten with snow on its nose and head, licking its nose. From Mammal Images Library by L.L. Master
American Marten (Martes americana). Image: Mammal Images Library by L.L. Master

Natural history collections are recognized repositories of molecular data, critical for measuring change through time. Historically, technology has had limited access the molecular secrets of aged specimens; however, high-throughput short-read sequencing has recently enhanced our ability to interrogate historical archives. Although specimen-derived DNA is not often amenable to long-read sequencing, creative reduced-representation genomic approaches that circumvent issues of DNA quality (e.g., RADsequ, exome capture) have catalyzed the field of museomics. New linked-read sequencing approaches (e.g., 10X Genomics) further enhance our ability to generate quality de novo genome assemblies from degraded specimens. These methods geographically connect short-reads in genome-space, creating assemblies with greater completeness and contiguity relative to shot-gun only assemblies. New technologies and the expanding availability quality reference assemblies from across the tree of life, increasingly enable comparative and population genomic studies that leverage the temporal depth and geographic breadth of museum archives. We use population-level genomic sampling across multiple species of Peromyscus (deer mice), a well-represented taxon in natural history collections, to identify genetic mechanisms of dehydration-tolerance. Desert-adapted deer mice may never drink water or urinate during their lifetime, yet they remain behaviorally and cognitively intact under extreme dehydration. In contrast, there are millions of dehydration-related deaths in humans each year. Identification of the genes and regulatory regions involved in desert adaptation in other mammals will help identify candidate loci for potential gene therapies in humans. A strong link between museums and public-health will bolster funding for these critical repositories and expand molecular applications. As the primary consumers of cryogenic tissue resources, it is the responsibility of the molecular biology community to contribute to the growth and maintenance of collections through the active contribution of biological resources via fieldwork or the incorporation of long-term specimen preservation costs into grant applications.

eric lopresti

Plants and the materials that stick to them: an ecological and evolutionary investigation

A predatory stiltbug (Jalysus wickhami) scavenges a dead fly caught and killed by the sticky plant Mentzelia micrantha.
A predatory stiltbug (Jalysus wickhami) scavenges a dead fly caught and killed by the sticky plant Mentzelia micrantha.

A pressed plant specimen in an herbarium has long been the source of morphological, chemical, genetic and other sorts of data on the plant. However, that physical specimen
also includes incidental collections of other material which can inform conclusions about the plant’s ecology and interactions. My research uses collections of sticky plants to study plant interactions by examining material that sticks to the plant during its lifetime; I have found sand, dead bugs, bird feathers and ash on the surfaces of plant specimens. My recent work has demonstrated that certain substances–biological or not–stuck to plants mediate both simple and complex interactions with both arthropods and mammals, resulting in major fitness implications for the plant. However, the ubiquity of these interactions is unknown. My research links the ecological functioning of sticky plant interactions with the breadth and evolutionary history of stickiness. I will detail ecological interactions of stickiness, broad patterns of stickiness across the plant phylogeny, as well as in more detail across a single clade of plants endemic to western North America.

alexis mychajliw

Conflicts in context: natural history collections as archives of human-carnivore interactions through time

grizzly bear specimen
California grizzly bear (Ursus arctos californicus), Smithsonian Museum of Natural History.

Human-wildlife conflict in both rural and urban areas is a persistent threat to the continued existence of many predators. Historically, mammalian carnivores have faced severe range contractions, but, in some places, they are naturally re-expanding or being reintroduced, accompanied by a range of political dilemmas and public misconceptions. In combination with traditional conservation studies of extant populations, I provide historic and pre-European baselines to anticipate these dilemmas and distinguish between novel behaviors versus the return of normal, pre-contraction variation. Museum collections (natural history, archaeological, and paleontological can provide unexpected spaces for policy-relevant dialogues among stakeholders and be at the center of interdisciplinary working groups including ecologists, paleontologists, historians, practitioners and social scientists. Employing a diverse range of geochemical, morphological and archival techniques in a conservation paleobiology framework, I have used museum collections to reframe public discourse on the reintroduction of grizzly bears to California, discover the first successful case of North American “Pleistocene rewilding” for carnivores from the 1930s, and evaluate how culturally important Japanese red foxes have responded to urbanization with attendant disease-transmission consequences. Given the cultural biases present in historical narratives of carnivore conflict, museum specimens provide an irreplaceable mechanism for separating perception from reality to guide real-world policy decisions, and museum exhibits themselves can be vehicles for communicating this new understanding.

daniel park

Herbarium collections reveal wide variation in plant phenological responses to climate

illustration showing thermometer, growing flower and stopwatch
Plants exhibit variable phenological responses to climate

Changes in phenology–the timing of life history events–are among the most dramatic biological responses to climate change. Herbarium specimens represent snapshots of phenology (i.e. flowering and fruiting) at a specific place and time, and have tremendous promise to increase the spatial, temporal and taxonomic resolution of phenological data. However, difficulties in extracting useful information from specimens efficiently have limited efforts to apply collections-based approaches to large-scale phenological research. Here we present two contrasting approaches for this purpose; crowdsourcing and machine learning; and discuss the promises and opportunities of applying specimen-derived data to phenological research. Using these approaches, we examined tens of thousands of specimens and uncovered substantial and unexpected variation in phenological sensitivity across species ranges. We also observe patterns of temporal convergence among closely related species when they co-occur. These results suggest that phenological responses to climate change will be heterogeneous within communities and across regions, with large amounts of regional variability driven by local adaptation, phenotypic plasticity and differences in species assemblages. We thus demonstrate the utility of natural history collections in revealing large-scale patterns within assemblages and across continents that ultimately can improve forecasts of climatic change impacts on the structure and function of ecosystems.

kelly speer

Determining drivers of symbiont evolution in a multi-tier hierarchical system

Bat flies hitching a ride on their host, Pteronotus parnelli.
Bat flies hitching a ride on their host, Pteronotus parnelli. Image: M. Brock Fenton and Sherri Fenton.

The use of natural history specimens is continually reimagined beyond the original intent with which they were collected. Recently, natural history specimens have been used to examine change in host-associated microbial communities through time in response to environmental change. Leveraging the inherent nestedness of host-parasite-microbiome assemblages to minimize sources of variation, I examine how the microbiomes of insect parasites change across space, time and environments, and assess the implications of these changes for pathogen prevalence. I focus on the bacterial microbiome of bat flies (Streblidae and Nycteribiidae), which are obligate, blood-feeding ectoparasites of bats, that vector pathogens to their hosts. I find that bat fly microbiomes are extremely specific to the species of fly they occupy regardless of abiotic factors. However, habitat fragmentation, time and geographic space also contribute to variation in the microbiome of bat flies. This variation is not correlated with prevalence of two arthropod-vectored pathogens of bats, but possibly strain-level occurrence. As greater interaction between humans and wildlife leads to increased zoonotic disease events, it is imperative to explore natural history collections as untapped sources of information about the progression of pathogen spread and corresponding wildlife microbiome change.

alex white

Biogeography of fern shapes as revealed by deep learning

Resurrection fern (Pleopeltis polypodioides) specimen silhouette; similar silhouettes are used to train deep learning models to analyze the shapes of fern specimens from across the globe.
Resurrection fern (Pleopeltis polypodioides) specimen silhouette; similar silhouettes are used to train deep learning models to analyze the shapes of fern specimens from across the globe.

With digitized herbarium specimens and associated metadata accumulating rapidly in open access repositories, we are now able to exploit data-hungry computer vision techniques in order to evaluate fundamental questions in plant evolution. High among the list of unknowns are the roles that ecological factors and morphological similarity play in mediating biogeographic patterns of taxonomic and phylogenetic diversity. Here, I integrate deep convolutional neural networks (CNNs) into a biogeographic study of morphological, taxonomic, and phylogenetic diversity in ferns and lycophytes. I show how CNNs and digitized specimens can be used to extract quantitative estimates of morphospace occupation, and I use these techniques to evaluate diversity-disparity relationships within ferns across latitudes. I also discuss how CNNs can be used to overcome logistical obstacles arising from modern specimen based workflows involving millions of images.

laurel yohe

Morphological and developmental basis of olfactory evolution: evidence from museum-collected iodine-stained bat specimens and embryos

Embryo series of the fig-eating bat Artibeus jamaicensis with olfactory tissue outlined in different colors. Note how the complexity of the olfactory turbinal shapes develop throughout ontogeny.
Embryo series of the fig-eating bat Artibeus jamaicensis with olfactory tissue outlined in different colors. Note how the complexity of the olfactory turbinal shapes develop throughout ontogeny.

The sense of smell is essential for finding food in animals, but whether olfaction has evolved in relation to diet is not understood. Animals that more heavily rely on smell should have increased olfactory tissue than those that rely on other senses, yet this assumption is rarely tested. I investigated whether smell was associated with diet in a group of neotropical leaf-nosed bats known for their dietary diversity. Using iodine-stained museum specimens of both adult and embryo bats, I quantified the olfactory epithelium of nasal turbinate bones in species with divergent diets. Embryo specimens were obtained from museum-deposited adult females unknown to be pregnant during accession, providing a wealth of new specimens unbeknownst to science. I tested whether plant-visiting have more well-developed olfactory epithelium compared to animal-feeding bats. I discovered: [1] two of the five turbinate bones have increased epithelium in plant-visiting bats; and [2] development of turbinates remains simple earlier in ontogeny, but the two bones with increased epithelium develop at very late stages in plant-visiting bats. This discovery suggests olfactory adaptation in plant-visiting bats, and the accompanying morphology occurs at late developmental stages, supporting the notion that natural selection acts upon phenotypes appearing later in ontogeny.


Rob guralnick

Sizing up new uses of natural history collections for ecogeography and global change biology

Slide showing spatial and temporal patterns of mammal and bird body size change using natural history collectionsAbstract
Body size is a key integrator trait because it influences nearly all aspects of organismal biology.  It has strong relationships with fitness, and is influenced by a number of biotic and abiotic factors, while also potentially functionally and structurally constrained. Given its central importance, body size has long been studied by ecologists and evolutionary biologists, including burgeoning interest in size change as a key response to global changes such as human predation and global warming. In this talk, I show the power of natural history collections to inform about long-standing and new questions about body size change broadly over space and time.  I will first describe efforts to compile and share millions of measurements that have routinely been taken by field vertebrate biologists, utilizing a growing informatics toolkit and semantic web approaches to make those available. I then provide four case studies, two focused on examining a classical ecogeographical rule, Bergmann’s Rule. The first case study takes an initial look at this rule across 1000s of vertebrate species. The second focuses on a narrower subset but examines multiple climate predictors, not just temperature, and asks if species climate niche determines intraspecific body size change. The third case study asks if we can use natural history collections to understand body size changes over the recent past and due to climatic factors and human population changes, focusing on a case study on deer mice across North America. Finally, I showcase the potential to look over very broad evolutionary time, and understand shape and size change of butterfly wings, again using the power of natural history collections, showcasing vastly different evolutionary rates for fore- and hindwing shape and size. I close noting the importance of building the infrastructure to support the concept of the extended specimen, as a transformational next step in facilitating novel use of natural history collections.​

pamela soltis

Integrative research using natural history collections: examples from herbaria

closeup of a magnolia tree leaves and seed pod
Magnolia macrophylla.

Emerging cyberinfrastructure and new data sources provide unparalleled opportunities for mobilizing and integrating massive amounts of information from organismal biology, ecology, genetics, climatology and other disciplines. Key among these data sources is the rapidly growing volume of digitized specimen records from natural history collections. The world’s herbaria house an estimated 400,000,000 specimens, and as the number of online records – currently at ~60,000,000 – continues to grow, these data provide excellent information on species distributions, changes in distributions over time, phenology and a host of traits. Integration of information from specimen records with phylogenies, climate data and other resources enables new questions to be addressed while also providing new perspectives on longstanding questions in ecology and evolutionary biology. Although challenges to linking heterogeneous data remain, new advances are enabling the use of herbarium and other museum data in novel ways. Through a series of case studies, I will illustrate some of the many uses to which herbarium specimen data are currently being applied as well as some of the resources being developed to enable their use. These case studies link and analyze specimen data and related heterogeneous data sources to address a range of evolutionary and ecological problems.