Ancient DNA confirms diverse origins of early post-Columbian cattle in the Americas.

Before the arrival of Europeans, domestic cattle (Bos taurus) did not exist in the Americas, and most of our knowledge about how domestic bovines first arrived in the Western Hemisphere is based on historical documents. Sixteenth-century colonial accounts suggest that the first cattle were brought in small numbers from the southern Iberian Peninsula via the Canary archipelago to the Caribbean islands where they were bred locally and imported to other circum-Caribbean regions. Modern American heritage cattle genetics and limited ancient mtDNA data from archaeological colonial cattle suggest a more complex story of mixed ancestries from Europe and Africa. So far little information exists to understand the nature and timing of the arrival of these mixed-ancestry populations. In this study we combine ancient mitochondrial and nuclear DNA from a robust sample of some of the earliest archaeological specimens from Caribbean and Mesoamerican sites to clarify the origins and the dynamics of bovine introduction into the Americas. Our analyses support first arrival of cattle from diverse locales and potentially confirm the early arrival of African-sourced cattle in the Americas, followed by waves of later introductions from various sources over several centuries.

Computer vision for assessing species color pattern variation from web-based community science images.

Openly available community science digital vouchers provide a wealth of data to study phenotypic change across space and time. However, extracting phenotypic data from these resources requires significant human effort. Here, we demonstrate a workflow and computer vision model for automatically categorizing species color pattern from community science images. Our work is focused on documenting the striped/unstriped color polymorphism in the Eastern Red-backed Salamander (Plethodon cinereus). We used an ensemble convolutional neural network model to analyze this polymorphism in 20,318 iNaturalist images. Our model was highly accurate (∼98%) despite image heterogeneity. We used the resulting annotations to document extensive niche overlap between morphs, but wider niche breadth for striped morphs at the range-wide scale. Our work showcases key design principles for using machine learning with heterogeneous community science image data to address questions at an unprecedented scale.

Analysis of the earliest complete mtDNA genome of a Caribbean colonial horse (Equus caballus) from 16th-century Haiti.

Unlike other European domesticates introduced in the Americas after the European invasion, equids (Equidae) were previously in the Western Hemisphere but were extinct by the late Holocene era. The return of equids to the Americas through the introduction of the domestic horse (Equus caballus) is documented in the historical literature but is not explored fully either archaeologically or genetically. Historical documents suggest that the first domestic horses were brought from the Iberian Peninsula to the Caribbean in the late 15th century CE, but archaeological remains of these early introductions are rare. This paper presents the mitochondrial genome of a late 16th century horse from the Spanish colonial site of Puerto Real (northern Haiti). It represents the earliest complete mitogenome of a post-Columbian domestic horse in the Western Hemisphere offering a unique opportunity to clarify the phylogeographic history of this species in the Americas. Our data supports the hypothesis of an Iberian origin for this early translocated individual and clarifies its phylogenetic relationship with modern breeds in the Americas.

Climate drivers of adult insect activity are conditioned by life history traits.

Insect phenological lability is key for determining which species will adapt under environmental change. However, little is known about when adult insect activity terminates and overall activity duration. We used community-science and museum specimen data to investigate the effects of climate and urbanisation on timing of adult insect activity for 101 species varying in life history traits. We found detritivores and species with aquatic larval stages extend activity periods most rapidly in response to increasing regional temperature. Conversely, species with subterranean larval stages have relatively constant durations regardless of regional temperature. Species extended their period of adult activity similarly in warmer conditions regardless of voltinism classification. Longer adult durations may represent a general response to warming, but voltinism data in subtropical environments are likely underreported. This effort provides a framework to address the drivers of adult insect phenology at continental scales and a basis for predicting species response to environmental change.

Ancient DNA from the extinct Haitian cave-rail (Nesotrochis steganinos) suggests a biogeographic connection between the Caribbean and Old World.

Worldwide decline in biodiversity during the Holocene has impeded a comprehensive understanding of pre-human biodiversity and biogeography. This is especially true on islands, because many recently extinct island taxa were morphologically unique, complicating assessment of their evolutionary relationships using morphology alone. The Caribbean remains an avian hotspot but was more diverse before human arrival in the Holocene. Among the recently extinct lineages is the enigmatic genus Nesotrochis, comprising three flightless species. Based on morphology, Nesotrochis has been considered an aberrant rail (Rallidae) or related to flufftails (Sarothruridae). We recovered a nearly complete mitochondrial genome of Nesotrochis steganinos from fossils, discovering that it is not a rallid but instead is sister to Sarothruridae, volant birds now restricted to Africa and New Guinea, and the recently extinct, flightless Aptornithidae of New Zealand. This result suggests a widespread or highly dispersive most recent common ancestor of the group. Prior to human settlement, the Caribbean avifauna had a far more cosmopolitan origin than is evident from extant species.

Climate, urbanization, and species traits interactively drive flowering duration.

A wave of green leaves and multi-colored flowers advances from low to high latitudes each spring. However, little is known about how flowering offset (i.e., ending of flowering) and duration of populations of the same species vary along environmental gradients. Understanding these patterns is critical for predicting the effects of future climate and land-use change on plants, pollinators, and herbivores. Here, we investigated potential climatic and landscape drivers of flowering onset, offset, and duration of 52 plant species with varying key traits. We generated phenology estimates using >270,000 community-science photographs and a novel presence-only phenometric estimation method. We found longer flowering durations in warmer areas, which is more obvious for summer-blooming species compared to spring-bloomers driven by their strongly differing offset dynamics. We also found that higher human population density and higher annual precipitation are associated with delayed flowering offset and extended flowering duration. Finally, offset of woody perennials was more sensitive than herbaceous species to both climate and urbanization drivers. Empirical forecast models suggested that flowering durations will be longer in 2030 and 2050 under representative concentration pathway (RCP) 8.5, especially for summer-blooming species. Our study provides critical insight into drivers of key flowering phenophases and confirms that Hopkins' Bioclimatic Law also applies to flowering durations for summer-blooming species and herbaceous spring-blooming species.

Transforming the study of organisms: Phenomic data models and knowledge bases.

The rapidly decreasing cost of gene sequencing has resulted in a deluge of genomic data from across the tree of life; however, outside a few model organism databases, genomic data are limited in their scientific impact because they are not accompanied by computable phenomic data. The majority of phenomic data are contained in countless small, heterogeneous phenotypic data sets that are very difficult or impossible to integrate at scale because of variable formats, lack of digitization, and linguistic problems. One powerful solution is to represent phenotypic data using data models with precise, computable semantics, but adoption of semantic standards for representing phenotypic data has been slow, especially in biodiversity and ecology. Some phenotypic and trait data are available in a semantic language from knowledge bases, but these are often not interoperable. In this review, we will compare and contrast existing ontology and data models, focusing on nonhuman phenotypes and traits. We discuss barriers to integration of phenotypic data and make recommendations for developing an operationally useful, semantically interoperable phenotypic data ecosystem.

Machine Learning Using Digitized Herbarium Specimens to Advance Phenological Research.

Machine learning (ML) has great potential to drive scientific discovery by harvesting data from images of herbarium specimens-preserved plant material curated in natural history collections-but ML techniques have only recently been applied to this rich resource. ML has particularly strong prospects for the study of plant phenological events such as growth and reproduction. As a major indicator of climate change, driver of ecological processes, and critical determinant of plant fitness, plant phenology is an important frontier for the application of ML techniques for science and society. In the present article, we describe a generalized, modular ML workflow for extracting phenological data from images of herbarium specimens, and we discuss the advantages, limitations, and potential future improvements of this workflow. Strategic research and investment in specimen-based ML methods, along with the aggregation of herbarium specimen data, may give rise to a better understanding of life on Earth.

Maximizing human effort for analyzing scientific images: A case study using digitized herbarium sheets.

PREMISE: Digitization and imaging of herbarium specimens provides essential historical phenotypic and phenological information about plants. However, the full use of these resources requires high-quality human annotations for downstream use. Here we provide guidance on the design and implementation of image annotation projects for botanical research. METHODS AND RESULTS: We used a novel gold-standard data set to test the accuracy of human phenological annotations of herbarium specimen images in two settings: structured, in-person sessions and an online, community-science platform. We examined how different factors influenced annotation accuracy and found that botanical expertise, academic career level, and time spent on annotations had little effect on accuracy. Rather, key factors included traits and taxa being scored, the annotation setting, and the individual scorer. In-person annotations were significantly more accurate than online annotations, but both generated relatively high-quality outputs. Gathering multiple, independent annotations for each image improved overall accuracy. CONCLUSIONS: Our results provide a best-practices basis for using human effort to annotate images of plants. We show that scalable community science mechanisms can produce high-quality data, but care must be taken to choose tractable taxa and phenophases and to provide informative training material.

Ancient DNA and high-resolution chronometry reveal a long-term human role in the historical diversity and biogeography of the Bahamian hutia.

Quaternary paleontological and archaeological evidence often is crucial for uncovering the historical mechanisms shaping modern diversity and distributions. We take an interdisciplinary approach using multiple lines of evidence to understand how past human activity has shaped long-term animal diversity in an island system. Islands afford unique opportunities for such studies given their robust fossil and archaeological records. Herein, we examine the only non-volant terrestrial mammal endemic to the Bahamian Archipelago, the hutia Geocapromys ingrahami. This capromyine rodent once inhabited many islands but is now restricted to several small cays. Radiocarbon dated fossils indicate that hutias were present on the Great Bahama Bank islands before humans arrived at AD ~800-1000; all dates from other islands post-date human arrival. Using ancient DNA from a subset of these fossils, along with modern representatives of Bahamian hutia and related taxa, we develop a fossil-calibrated phylogeny. We found little genetic divergence among individuals from within either the northern or southern Bahamas but discovered a relatively deep North-South divergence (~750 ka). This result, combined with radiocarbon dating and archaeological evidence, reveals a pre-human biogeographic divergence, and an unexpected human role in shaping Bahamian hutia diversity and biogeography across islands.

Methods for broad-scale plant phenology assessments using citizen scientists' photographs.

PREMISE: Citizen science platforms for sharing photographed digital vouchers, such as iNaturalist, are a promising source of phenology data, but methods and best practices for use have not been developed. Here we introduce methods using Yucca flowering phenology as a case study, because drivers of Yucca phenology are not well understood despite the need to synchronize flowering with obligate pollinators. There is also evidence of recent anomalous winter flowering events, but with unknown spatiotemporal extents. METHODS: We collaboratively developed a rigorous, consensus-based approach for annotating and sharing whole plant and flower presence data from iNaturalist and applied it to Yucca records. We compared spatiotemporal flowering coverage from our annotations with other broad-scale monitoring networks (e.g., the National Phenology Network) in order to determine the unique value of photograph-based citizen science resources. RESULTS: Annotations from iNaturalist were uniquely able to delineate extents of unusual flowering events in Yucca. These events, which occurred in two different regions of the Desert Southwest, did not appear to disrupt the typical-period flowering. DISCUSSION: Our work demonstrates that best practice approaches to scoring iNaturalist records provide fine-scale delimitation of phenological events. This approach can be applied to other plant groups to better understand how phenology responds to changing climate.

The effect of urbanization on plant phenology depends on regional temperature.

Plant and animal phenology is shifting in response to urbanization, with most hypotheses focusing on the 'urban heat island' (UHI) effect as the driver. However, generalities regarding the direction and magnitude of phenological response to urbanization have not yet emerged because most studies have focused on remote-sensed vegetative phenologies or at local scales with relatively few species. Furthermore, how urbanization interacts with broad-scale climate gradients remains an unknown but important component of anthropogenically driven phenological change. Here, we used a database with >22 million in situ plant phenological observations from the United States and Europe to study the joint influence of varying human population density, which serves as an urbanization measure, and of regional temperature on median flowering and leaf-out dates across a wide plant phylogenetic spectrum. Separately, increasing population density and warmer regional temperature both advanced plant flowering and leaf-out. However, the influence of human population density on plant flowering and leaf-out depends on the regional temperature: high population density advanced plant phenology in cold areas but this effect disappeared or even reversed in warm areas. UHI effects (as measured by daily land surface temperature) alone cannot explain the overall influence of urbanization on plant phenology, suggesting that urbanization also affects plant phenology via other mechanisms. Shorter plants with large specific leaf areas and early flower or leaf-out dates were most affected by urbanization and temperature changes. Our study provides strong empirical evidence that the influence of urbanization on plant phenology varies with regional temperature. Therefore, robust understanding and accurate prediction of phenological changes must take this interaction into account.

Integrating herbarium specimen observations into global phenology data systems.

PREMISE OF THE STUDY: The Plant Phenology Ontology (PPO) was originally developed to integrate phenology observations of whole plants across different global observation networks. Here we describe a new release of the PPO and associated data pipelines that supports integration of phenology observations from herbarium specimens, which provide historical and modern phenology data. METHODS AND RESULTS: Critical changes to the PPO include key terms that describe how measurements from parts of plants, which are captured in most imaged herbarium specimens, relate to whole plants. We provide proof of concept for ingesting annotations from imaged herbarium sheets of Prunus serotina, the common black cherry. We then provide an example analysis of changes in flowering timing over the past 125 years, demonstrating the value of integrating herbarium and observational phenology data sets. CONCLUSIONS: These conceptual and technical advances will support the addition of phenology data from herbaria, but also could be expanded upon to facilitate the inclusion of data from photograph-based citizen science platforms. With the incorporation of herbarium phenology data, new historical baseline data will strengthen the capability to monitor, model, and forecast plant phenology changes.

Developing a vocabulary and ontology for modeling insect natural history data: example data, use cases, and competency questions.

Insects are possibly the most taxonomically and ecologically diverse class of multicellular organisms on Earth. Consequently, they provide nearly unlimited opportunities to develop and test ecological and evolutionary hypotheses. Currently, however, large-scale studies of insect ecology, behavior, and trait evolution are impeded by the difficulty in obtaining and analyzing data derived from natural history observations of insects. These data are typically highly heterogeneous and widely scattered among many sources, which makes developing robust information systems to aggregate and disseminate them a significant challenge. As a step towards this goal, we report initial results of a new effort to develop a standardized vocabulary and ontology for insect natural history data. In particular, we describe a new database of representative insect natural history data derived from multiple sources (but focused on data from specimens in biological collections), an analysis of the abstract conceptual areas required for a comprehensive ontology of insect natural history data, and a database of use cases and competency questions to guide the development of data systems for insect natural history data. We also discuss data modeling and technology-related challenges that must be overcome to implement robust integration of insect natural history data.

The Plant Phenology Ontology: A New Informatics Resource for Large-Scale Integration of Plant Phenology Data.

Plant phenology - the timing of plant life-cycle events, such as flowering or leafing out - plays a fundamental role in the functioning of terrestrial ecosystems, including human agricultural systems. Because plant phenology is often linked with climatic variables, there is widespread interest in developing a deeper understanding of global plant phenology patterns and trends. Although phenology data from around the world are currently available, truly global analyses of plant phenology have so far been difficult because the organizations producing large-scale phenology data are using non-standardized terminologies and metrics during data collection and data processing. To address this problem, we have developed the Plant Phenology Ontology (PPO). The PPO provides the standardized vocabulary and semantic framework that is needed for large-scale integration of heterogeneous plant phenology data. Here, we describe the PPO, and we also report preliminary results of using the PPO and a new data processing pipeline to build a large dataset of phenology information from North America and Europe.

Digitization protocol for scoring reproductive phenology from herbarium specimens of seed plants.

PREMISE OF THE STUDY: Herbarium specimens provide a robust record of historical plant phenology (the timing of seasonal events such as flowering or fruiting). However, the difficulty of aggregating phenological data from specimens arises from a lack of standardized scoring methods and definitions for phenological states across the collections community. METHODS AND RESULTS: To address this problem, we report on a consensus reached by an iDigBio working group of curators, researchers, and data standards experts regarding an efficient scoring protocol and a data-sharing protocol for reproductive traits available from herbarium specimens of seed plants. The phenological data sets generated can be shared via Darwin Core Archives using the Extended MeasurementOrFact extension. CONCLUSIONS: Our hope is that curators and others interested in collecting phenological trait data from specimens will use the recommendations presented here in current and future scoring efforts. New tools for scoring specimens are reviewed.

Eavesdropping to Find Mates: The Function of Male Hearing for a Cicada-Hunting Parasitoid Fly, Emblemasoma erro (Diptera: Sarcophagidae).

Females of several species of dipteran parasitoids use long-range hearing to locate hosts for their offspring by eavesdropping on the acoustic mating calls of other insects. Males of these acoustic eavesdropping parasitoids also have physiologically functional ears, but so far, no adaptive function for male hearing has been discovered. I investigated the function of male hearing for the sarcophagid fly Emblemasoma erro Aldrich, an acoustic parasitoid of cicadas, by testing the hypothesis that both male and female E. erro use hearing to locate potential mates. I found that both male and nongravid female E. erro perform phonotaxis to the sounds of calling cicadas, that male flies engage in short-range, mate-finding behavior once they arrive at a sound source, and that encounters between females and males at a sound source can lead to copulation. Thus, cicada calling songs appear to serve as a mate-finding cue for both sexes of E. erro Emblemasoma erro's mate-finding behavior is compared to that of other sarcophagid flies, other acoustic parasitoids, and nonacoustic eavesdropping parasitoids.

Infection behavior, life history, and host parasitism rates of Emblemasoma erro (Diptera: Sarcophagidae), an acoustically hunting parasitoid of the cicada Tibicen dorsatus (Hemiptera: Cicadidae).

BACKGROUND: 'Eavesdropping' parasitoids find their hosts by homing in on the communication signals of other insects. These parasitoids often exploit chemical communication, but at least some species of the sarcophagid genusEmblemasomaeavesdropon the acoustic communications of cicadas. Despite considerable scientific interest in acoustic parasitoids, we know remarkably little about most species of Emblemasoma. To better understand the ecology and behavioral diversity of these flies, I used a combination of field and laboratory techniques to elucidate theinfection behavior and life history of E.erro,which uses the cicada Tibicen dorsatusasa host, and I also investigated parasitoid loads and parasitism rates of T.dorsatus inmultiple host populations in the central United States. RESULTS: Female E. erro used the acoustic signals of male T. dorsatus as the primary means of locating hosts, but they also required physical movement by the host, usually either walking or flight, to provide visual cues for the final larviposition attack. Larvae were deposited directly on the host's integument and burrowed through intersegmental membrane to enter the host's body. On average, E. erro larvae spent 88.0 h residing inside their host before leaving to pupariate, but residence time was strongly dependent on both ambient temperature and effective clutch size. Adult flies eclosed about 18 days after pupariation. Across all study sites, the mean parasitoid load of infected male T. dorsatus was 4.97 larvae/host, and the overall parasitism rate was 26.3%. Parasitism rates and parasitoid loads varied considerably amonghost population samples, and high parasitism rates were usually associated with high parasitoid loads. CONCLUSIONS: Previously, detailed information about the infection behavior, life history, and host parasitism rates of sarcophagid acoustic parasitoids was only available for one species, E. auditrix. This study reveals that the infection behavior of E. erro is quite different from that of E. auditrix and, more broadly, unlike that known for any other species of acoustic parasitoid. The life histories of these two Emblemasoma are also divergent. These differences suggest that sarcophagid acoustic parasitoids are more behaviorally and ecologically diverse than previously recognized and in need of further study.

The trouble with triplets in biodiversity informatics: a data-driven case against current identifier practices.

The biodiversity informatics community has discussed aspirations and approaches for assigning globally unique identifiers (GUIDs) to biocollections for nearly a decade. During that time, and despite misgivings, the de facto standard identifier has become the "Darwin Core Triplet", which is a concatenation of values for institution code, collection code, and catalog number associated with biocollections material. Our aim is not to rehash the challenging discussions regarding which GUID system in theory best supports the biodiversity informatics use case of discovering and linking digital data across the Internet, but how well we can link those data together at this moment, utilizing the current identifier schemes that have already been deployed. We gathered Darwin Core Triplets from a subset of VertNet records, along with vertebrate records from GenBank and the Barcode of Life Data System, in order to determine how Darwin Core Triplets are deployed "in the wild". We asked if those triplets follow the recommended structure and whether they provide an easy and unambiguous means to track from specimen records to genetic sequence records. We show that Darwin Core Triplets are often riddled with semantic and syntactic errors when deployed and curated in practice, despite specifications about how to construct them. Our results strongly suggest that Darwin Core Triplets that have not been carefully curated are not currently serving a useful role for relinking data. We briefly consider needed next steps to overcome current limitations.

The BiSciCol Triplifier: bringing biodiversity data to the Semantic Web.

BACKGROUND: Recent years have brought great progress in efforts to digitize the world's biodiversity data, but integrating data from many different providers, and across research domains, remains challenging. Semantic Web technologies have been widely recognized by biodiversity scientists for their potential to help solve this problem, yet these technologies have so far seen little use for biodiversity data. Such slow uptake has been due, in part, to the relative complexity of Semantic Web technologies along with a lack of domain-specific software tools to help non-experts publish their data to the Semantic Web. RESULTS: The BiSciCol Triplifier is new software that greatly simplifies the process of converting biodiversity data in standard, tabular formats, such as Darwin Core-Archives, into Semantic Web-ready Resource Description Framework (RDF) representations. The Triplifier uses a vocabulary based on the popular Darwin Core standard, includes both Web-based and command-line interfaces, and is fully open-source software. CONCLUSIONS: Unlike most other RDF conversion tools, the Triplifier does not require detailed familiarity with core Semantic Web technologies, and it is tailored to a widely popular biodiversity data format and vocabulary standard. As a result, the Triplifier can often fully automate the conversion of biodiversity data to RDF, thereby making the Semantic Web much more accessible to biodiversity scientists who might otherwise have relatively little knowledge of Semantic Web technologies. Easy availability of biodiversity data as RDF will allow researchers to combine data from disparate sources and analyze them with powerful linked data querying tools. However, before software like the Triplifier, and Semantic Web technologies in general, can reach their full potential for biodiversity science, the biodiversity informatics community must address several critical challenges, such as the widespread failure to use robust, globally unique identifiers for biodiversity data.