Increasing the impact of vertebrate scientific collections through 3D imaging: The openVertebrate (oVert) Thematic Collections Network.

The impact of preserved museum specimens is transforming and increasing by three-dimensional (3D) imaging that creates high-fidelity online digital specimens. Through examples from the openVertebrate (oVert) Thematic Collections Network, we describe how we created a digitization community dedicated to the shared vision of making 3D data of specimens available and the impact of these data on a broad audience of scientists, students, teachers, artists, and more. High-fidelity digital 3D models allow people from multiple communities to simultaneously access and use scientific specimens. Based on our multiyear, multi-institution project, we identify significant technological and social hurdles that remain for fully realizing the potential impact of digital 3D specimens.

Interspecific hybridization explains rapid gorget colour divergence in Heliodoxa hummingbirds (Aves: Trochilidae).

Hybridization is a known source of morphological, functional and communicative signal novelty in many organisms. Although diverse mechanisms of established novel ornamentation have been identified in natural populations, we lack an understanding of hybridization effects across levels of biological scales and upon phylogenies. Hummingbirds display diverse structural colours resulting from coherent light scattering by feather nanostructures. Given the complex relationship between feather nanostructures and the colours they produce, intermediate coloration does not necessarily imply intermediate nanostructures. Here, we characterize nanostructural, ecological and genetic inputs in a distinctive Heliodoxa hummingbird from the foothills of eastern Peru. Genetically, this individual is closely allied with Heliodoxa branickii and Heliodoxa gularis, but it is not identical to either when nuclear data are assessed. Elevated interspecific heterozygosity further suggests it is a hybrid backcross to H. branickii. Electron microscopy and spectrophotometry of this unique individual reveal key nanostructural differences underlying its distinct gorget colour, confirmed by optical modelling. Phylogenetic comparative analysis suggests that the observed gorget coloration divergence from both parentals to this individual would take 6.6-10 My to evolve at the current rate within a single hummingbird lineage. These results emphasize the mosaic nature of hybridization and suggest that hybridization may contribute to the structural colour diversity found across hummingbirds.

Climate change affects bird nesting phenology: Comparing contemporary field and historical museum nesting records.

Global climate change impacts species and ecosystems in potentially harmful ways. For migratory bird species, earlier spring warm-up could lead to a mismatch between nesting activities and food availability. CO2 provides a useful proxy for temperature and an environmental indicator of climate change when temperature data are not available for an entire time series. Our objectives were to (a) examine nesting phenology over time; (b) determine how nesting phenology relates to changes in atmospheric CO2 concentration; and (c) demonstrate the usefulness of historical museum collections combined with modern observations for trend analyses. We assessed changes in nesting dates of 72 bird species in the Upper Midwest of the United States by comparing contemporary lay dates with those obtained from archived, historical museum nest records over a 143-year period (1872-2015). Species-specific changes in lay date per one unit change in the CO2 residual ranged from -0.75 (95% CI: -1.57 to -0.10) to 0.45 (95% CI: -0.29 to 1.43). Overall, lay dates advanced ~10 days over the 143-year period. Resident, short-distance migrants and long-distance migrants lay dates advanced by ~15, 18 and 16 days on average respectively. Twenty-four species (33.3%) significantly advanced, one (1.4%) significantly delayed and we failed to detect an advance or delay in lay date for 47 species (65.3%). Overall mean advance in first lay date (for the species that have significantly advanced laying date) was 25.1 days (min: 10.7, max: 49.9). Our study highlights the scientific importance of both data gathering and archiving through time to understand phenological change. The detailed archived information reported by egg collectors provide the early data of our study. As with studies of egg-shell thinning and pesticide exposure, our use of these data illustrates another scientific utility of egg collections that these pioneer naturalists never imagined. As museums archive historical data, these locations are also ideal candidates to store contemporary field data as it is collected. Together, such information will provide the ability to track, understand and perhaps predict responses to human-driven environmental change.

Climatic refugia and reduced extinction correlate with underdispersion in mammals and birds in Africa.

Macroevolutionary patterns, often inferred from metrics of community relatedness, are often used to ascertain major evolutionary processes shaping communities. These patterns have been shown to be informative of biogeographic barriers, of habitat suitability and invasibility (especially with regard to environmental filtering), and of regions that function as evolutionary cradles (i.e., sources of diversification) or museums (i.e., regions of reduced extinction). Here, we analyzed continental datasets of mammal and bird distributions to identify primary drivers of community evolution on the African continent for mostly endothermic vertebrates. We find that underdispersion (i.e., relatively low phylogenetic diversity compared to species richness) closely correlates with specific ecoregions that have been identified as climatic refugia in the literature, regardless of whether these specific regions have been touted as cradles or museums. Using theoretical models of identical communities that differ only with respect to extinction rates, we find that even small suppressions of extinction rates can result in underdispersed communities, supporting the hypothesis that climatic stability can lead to underdispersion. We posit that large-scale patterns of under- and overdispersion between regions of similar species richness are more reflective of a particular region's extinction potential, and that the very nature of refugia can lead to underdispersion via the steady accumulation of species richness through diversification within the same ecoregion during climatic cycles. Thus, patterns of environmental filtering can be obfuscated by environments that coincide with biogeographic refugia, and considerations of regional biogeographic history are paramount for inferring macroevolutionary processes.

The Complete Genome Sequence of Conuropsis carolinensis, the Carolina Parakeet.

The Carolina Parakeet (Conuropsis carolinensis) is an extinct species of parrot that was native to the eastern, midwest, and plains regions of the United States. We present the whole genome sequence of this species. Illumina sequencing was performed on a genetic sample from a single captive individual. The reads were assembled using a de novo method followed by a series of references from related species for finishing. The raw and assembled data is publicly available via Genbank: Sequence Read Archive (SRR21023482) and assembled genome (JAOBYI000000000).

Repeated sampling of individuals reveals impact of tropical and temperate habitats on microbiota of a migratory bird.

Migratory animals experiencing substantial change in diet and habitat across the annual cycle may have corresponding shifts in host-associated microbial diversity. Using automated telemetry and radio tags to recapture birds, we examined gut microbiota structure in the same population and often same individual of Kirtland's Warblers (Setophaga kirtlandii) initially sampled on their wintering grounds in The Bahamas and subsequently resampled within their breeding territories in Michigan, USA. Initial sampling occurred in March and April and resampling occurred in May, June and early July. The composition of the most abundant phyla and classes of the warblers' microbiota is similar to that of other migratory birds. However, we detected notable variation in abundance and diversity of numerous bacterial taxa, including a decrease in microbial richness and significant differences in microbial communities when comparing the microbiota of birds first captured in The Bahamas to that of birds recaptured in Michigan. This is observed at the individual and population level. Furthermore, we found that 22 bacterial genera exhibit heightened abundance within specific sampling periods and are probably associated with diet and environmental change. Finally, we described a small, species-specific shared microbial profile that spans multiple time periods and environments within the migratory cycle. Our research highlights that the avian gut microbiota is dynamic over time, most significantly impacted by changing environments associated with migration. These results support the need for full annual cycle monitoring of migratory bird microbiota to improve understanding of seasonal host movement ecologies and response to recurrent physiological stressors.

Contrasting drivers of diversity in hosts and parasites across the tropical Andes.

Geographic turnover in community composition is created and maintained by eco-evolutionary forces that limit the ranges of species. One such force may be antagonistic interactions among hosts and parasites, but its general importance is unknown. Understanding the processes that underpin turnover requires distinguishing the contributions of key abiotic and biotic drivers over a range of spatial and temporal scales. Here, we address these challenges using flexible, nonlinear models to identify the factors that underlie richness (alpha diversity) and turnover (beta diversity) patterns of interacting host and parasite communities in a global biodiversity hot spot. We sampled 18 communities in the Peruvian Andes, encompassing ∼1,350 bird species and ∼400 hemosporidian parasite lineages, and spanning broad ranges of elevation, climate, primary productivity, and species richness. Turnover in both parasite and host communities was most strongly predicted by variation in precipitation, but secondary predictors differed between parasites and hosts, and between contemporary and phylogenetic timescales. Host communities shaped parasite diversity patterns, but there was little evidence for reciprocal effects. The results for parasite communities contradicted the prevailing view that biotic interactions filter communities at local scales while environmental filtering and dispersal barriers shape regional communities. Rather, subtle differences in precipitation had strong, fine-scale effects on parasite turnover while host-community effects only manifested at broad scales. We used these models to map bird and parasite turnover onto the ecological gradients of the Andean landscape, illustrating beta-diversity hot spots and their mechanistic underpinnings.

Dispersal ability correlates with range size in Amazonian habitat-restricted birds.

Understanding how species attain their geographical distributions and identifying traits correlated with range size are important objectives in biogeography, evolutionary biology and biodiversity conservation. Despite much effort, results have been varied and general trends have been slow to emerge. Studying species pools that occupy specific habitats, rather than clades or large groupings of species occupying diverse habitats, may better identify ranges size correlates and be more informative for conservation programmes in a rapidly changing world. We evaluated correlations between a set of organismal traits and range size in bird species from Amazonian white-sand ecosystems. We assessed if results are consistent when using different data sources for phylogenetic and range hypotheses. We found that dispersal ability, as measured by the hand-wing index, was correlated with range size in both white-sand birds and their non-white-sand sister taxa. White-sand birds had smaller ranges on average than their sister taxa. The results were similar and robust to the different data sources. Our results suggest that the patchiness of white-sand ecosystems limits species' ability to reach new habitat islands and establish new populations.

Sonations in Migratory and Non-migratory Fork-tailed Flycatchers (Tyrannus savana).

Sonations are sounds that animals produce with structures other than the vocal apparatus for communication. In birds, many sonations are usually produced with modified flight feathers through diverse kinematic mechanisms. For instance, aeroelastic fluttering of feathers produces tonal sound when airflow exceeds a threshold velocity and induces flight feathers to oscillate at a constant frequency. The Fork-tailed flycatcher (Tyrannus savana) is a Neotropical bird with both migratory and year-round resident subspecies that differ in the shape of the outer primary feathers of their wings. By integrating behavioral observations, audio recordings, and high-speed videos, we find that male Fork-tailed flycatchers produce sonations with their outer primary feathers P8-10, and possibly P7. These sounds are produced during different behavioral contexts including: the pre-dawn display, intraspecific territorial disputes, when attacking potential nest predators, and when escaping. By placing feathers in a wind tunnel, we elicited flutter at frequencies that matched the acoustic signature of sounds recorded in the wild, indicating that the kinematic mechanism responsible for sound production is aeroelastic flutter. Video of wild birds indicated that sonations were produced during the downstroke. Finally, the feathers of migratory (T.s.savana) and year-round resident (T.s.monachus) Fork-tailed flycatchers flutter in feather locations that differ in shape between the subspecies, and these shape differences between the subspecies result in sounds produced at different frequencies.

Andean Tectonics and Mantle Dynamics as a Pervasive Influence on Amazonian Ecosystem.

The Amazonian landscape evolution is the result of the combined effect of Andean tectonism, climate and the Earth's interior dynamics. To reconstruct the landscape evolution and its influence on paleoenvironmental variations within Amazonia since the Oligocene, we conducted numerical experiments that incorporate different surface and geodynamic processes, reproducing many paleogeographic features as inferred from the sedimentary record. We show that the evolution of the drainage pattern gradually reduced the area of sedimentation derived from the Guiana and Brazilian shields while expanded the Andean derived deposits during the Miocene, affecting the nutrient availability. First order biotic habitats were inferred from these paleogeographical reconstructions, showing an eastward expansion of várzea and terra firme forests and consequent retraction of igapó forests, with a millennial-scale reconfiguration of a mosaic of habitats in the lowlands. We conclude that this dynamism probably guided the observed patterns of speciation in the most biodiverse biome on Earth.

Evidence for mtDNA capture in the jacamar Galbula leucogastra/chalcothorax species-complex and insights on the evolution of white-sand ecosystems in the Amazon basin.

Jacamar species occur throughout Amazonia, with most species occupying forested habitats. One species-complex, Galbula leucogastra/chalcothorax, is associated to white sand ecosystems (WSE). Previous studies of WSE bird species recovered shallow genetic structure in mtDNA coupled with signs of gene flow among WSE patches. Here, we characterize diversification of the G. leucogastra/chalcothorax species-complex with dense sampling across its distribution using mitochondrial and genomic (Ultraconserved Elements, UCEs) DNA sequences. We performed concatenated likelihood and Bayesian analysis, as well as a species-tree analysis using ∗BEAST, to establish the phylogenetic relationships among populations. The mtDNA results recovered at least six geographically-structured lineages, with G. chalcothorax embedded within lineages of G. leucogastra. In contrast, both concatenated and species-tree analyses of UCE data recovered G. chalcothorax as sister to all G. leucogastra lineages. We hypothesize that the mitochondrial genome of one of the G. leucogastra lineage (Madeira) was captured into G. chalcothorax in the past. We discuss how WSE evolution and the coevolution of mtDNA and nuclear genes might have played a role in this apparently rare event.

Connecting Amazonian, Cerrado, and Atlantic forest histories: Paraphyly, old divergences, and modern population dynamics in tyrant-manakins (Neopelma/Tyranneutes, Aves: Pipridae).

Several biogeographic hypotheses have been proposed to explain connections between Amazonian and Atlantic forest biotas. These hypotheses are related to the timing of the connections and their geographic patterns. We performed a phylogeographic investigation of Tyrant-manakins (Aves: Pipridae, Neopelma/Tyranneutes) which include species inhabiting the Amazon and Atlantic forests, as well as gallery forests of the Cerrado. Using DNA sequence data, we determined phylogenetic relationships, temporal and geographic patterns of diversification, and recent intraspecific population genetic patterns, relative to the history of these biomes. We found Neopelma to be a paraphyletic genus, as N. chrysolophum is sister to Neopelma + Tyranneutes, with an estimated divergence of approximately 18 Myrs BP, within the oldest estimated divergence times of other Amazonian and Atlantic forest avian taxa. Subsequent divergences in the group occurred from Mid Miocene to Early Pliocene and involved mainly the Amazonian species, with an expansion into and subsequent speciation in the Cerrado gallery forests by N. pallescens. We found additional structure within N. chrysocephalum and N. sulphureiventer. Analysis of recent population dynamics in N. chrysocephalum, N. sulphureiventer, and N. pallescens revealed recent demographic fluctuations and restrictions to gene flow related to environmental changes since the last glacial cycle. No genetic structure was detected across the Amazon River in N. pallescens. The tyrant-manakins represent an old historical connection between the Amazon and Atlantic Forest.

Phylogenetic relationships of weaverbirds (Aves: Ploceidae): A first robust phylogeny based on mitochondrial and nuclear markers.

Weaverbirds are a diverse passerine group with species diversity concentrated in sub-Saharan Africa. No comprehensive phylogenetic hypothesis regarding relationships of weaverbirds has been produced, however, so we developed a first extensive phylogeny for the family Ploceidae, based on a multilocus dataset of three mitochondrial loci and four nuclear markers. Analysis of these data offered strong support for monophyly of the family and revealed seven distinct clades within Ploceidae. A major feature of our results is broad polyphyly of Ploceus: Asian Ploceus species should retain the generic name, whereas African Ploceus, together with Anaplectes, should be placed in Malimbus. In light of deep divergence, we assign the Malagasy Ploceus species to their own genus, Nelicurvius. Divergence time analysis based on DNA substitution rates suggests a mid-Miocene origin of the family. This study lays a foundation for an array of future studies of character evolution, biogeography, and evolutionary history of the family.

Sex in the City: Breeding Behavior of Urban Peregrine Falcons in the Midwestern US.

Peregrine falcons (Falco peregrinus) were extirpated from most of the continental United States by widespread use of the pesticide DDT in the 1960s. Populations have rebounded with banning of the pesticide and successful implementation of captive breeding and hacking programs. An essentially new population of Midwestern peregrines now exists that is comprised almost entirely of urban-nesting birds. The new population is considered to be of mixed ancestry, occurs at relatively high densities, and has nest sites in close proximity, factors that could influence breeding behaviors including mate fidelity, nest-site fidelity, extra-pair paternity, and natal dispersal. We investigated these behaviors using a combination of field observations and DNA microsatellite genotyping. Data for eleven microsatellite DNA markers, including eight newly developed for the species, were analyzed from a total of 350 birds from nine Midwestern cities, representing 149 broods collected at 20 nest sites. To document breeding behavior, parentage was inferred by likelihood techniques when both parents were sampled and by parental genotype reconstruction when only one parent was sampled. In cases where neither parent was sampled, a sibship reconstruction approach was used. We found high mate fidelity and nest-site fidelity in urban peregrines; in 122 nesting attempts made by long-term breeders, only 12 (9.8%) mate changes and six (4.9%) nest-site changes occurred. Only one brood (of 35 tested) revealed extra-pair paternity and involved a male tending two offspring of a recently acquired mate. Natal dispersal patterns indicated that female peregrines dispersed on average 226 km, almost twice the distance of males (average 124 km). Despite the novel environment of cities, our results suggest that monogamous breeding, nest fidelity, and female natal dispersal are high in urban peregrines, not unlike other raptors living in non-urban habitats.

Molecular systematics of the new world screech-owls (Megascops: Aves, Strigidae): biogeographic and taxonomic implications.

Megascops screech-owls are endemic to the New World and range from southern Canada to the southern cone of South America. The 22 currently recognized Megascops species occupy a wide range of habitats and elevations, from desert to humid montane forest, and from sea level to the Andean tree line. Species and subspecies diagnoses of Megascops are notoriously difficult due to subtle plumage differences among taxa with frequent plumage polymorphism. Using three mitochondrial and three nuclear genes we estimated a phylogeny for all but one Megascops species. Phylogenies were estimated with Maximum Likelihood and Bayesian Inference, and a Bayesian chronogram was reconstructed to assess the spatio-temporal context of Megascops diversification. Megascops was paraphyletic in the recovered tree topologies if the Puerto Rican endemic M. nudipes is included in the genus. However, the remaining taxa are monophyletic and form three major clades: (1) M. choliba, M. koepckeae, M. albogularis, M. clarkii, and M. trichopsis; (2) M. petersoni, M. marshalli, M. hoyi, M. ingens, and M. colombianus; and (3) M. asio, M. kennicottii, M. cooperi, M. barbarus, M. sanctaecatarinae, M. roboratus, M. watsonii, M. atricapilla, M. guatemalae, and M. vermiculatus. Megascops watsonii is paraphyletic with some individuals more closely related to M. atricapilla than to other members in that polytypic species. Also, allopatric populations of some other Megascops species were highly divergent, with levels of genetic differentiation greater than between some recognized species-pairs. Diversification within the genus is hypothesized to have taken place during the last 8 million years, with a likely origin in Central America. The genus later expanded over much of the Americas and then diversified via multiple dispersal events from the Andes into the Neotropical lowlands.

Inferring speciation history in the Andes with reduced-representation sequence data: an example in the bay-backed antpittas (Aves; Grallariidae; Grallaria hypoleuca s. l.).

In the Andes, humid-forest organisms frequently exhibit pronounced genetic structure and geographic variation in phenotype, often coincident with physical barriers to dispersal. However, phylogenetic relationships of clades have often been difficult to resolve due to short internodes. Consequently, even in taxa with well-defined genetic structure, the temporal and geographic sequences of dispersal and vicariance events that led to this differentiation have remained opaque, hindering efforts to test the association between diversification and earth history and to understand the assembly of species-rich communities on Andean slopes. Here, we use mitochondrial DNA and thousands of short-read sequences generated with genotyping by sequencing (GBS) to examine the geographic history of speciation in a lineage of passerine birds found in the humid forest of the Andes, the 'bay-backed' antpitta complex (Grallaria hypoleuca s. l). Mitochondrial DNA genealogies documented genetic structure among clade but were poorly resolved at nodes relevant for biogeographic inference. By contrast, relationships inferred from GBS loci were highly resolved and suggested a biogeographic history in which the ancestor originated in the northern Andes and dispersed south. Our results are consistent with a scenario of vicariant speciation wherein the range of a widespread ancestor was fragmented as a result of geologic or climatic change, rather than a stepping-stone series of dispersal events across pre-existing barriers. However, our study also highlights challenges of distinguishing dispersal-mediated speciation from static vicariance. Our results further demonstrate the substantial evolutionary timescale over which the diverse biota of the Andes was assembled.

Potential merger of ancient lineages in a passerine bird discovered based on evidence from host-specific ectoparasites.

The merger of formerly isolated lineages is hypothesized to occur in vertebrates under certain conditions. However, despite many demonstrated instances of introgression between taxa in secondary contact, examples of lineage mergers are rare. Preliminary mtDNA sequencing of a Malagasy passerine, Xanthomixis zosterops (Passeriformes: Bernieridae), indicated a possible instance of merging lineages. We tested the hypothesis that X. zosterops lineages are merging by comparing mtDNA sequence and microsatellite data, as well as mtDNA sequence data from host-specific feather lice in the genus Myrsidea (Phthiraptera: Menoponidae). Xanthomixis zosterops comprises four deeply divergent, broadly sympatric, cryptic mtDNA clades that likely began diverging approximately 3.6 million years ago. Despite this level of divergence, the microsatellite data indicate that the X. zosterops mtDNA clades are virtually panmictic. Three major phylogroups of Myrsidea were found, supporting previous allopatry of the X. zosterops clades. In combination, the datasets from X. zosterops and its Myrsidea document a potential merger of previously allopatric lineages that likely date to the Pliocene. This represents the first report of sympatric apparent hybridization among more than two terrestrial vertebrate lineages. Further, the mtDNA phylogeographic pattern of X. zosterops, namely the syntopy of more than two deeply divergent cryptic clades, appears to be a novel scenario among vertebrates. We highlight the value of gathering multiple types of data in phylogeographic studies to contribute to the study of vertebrate speciation.

Divergence at the edges: peripatric isolation in the montane spiny throated reed frog complex.

BACKGROUND: Peripatric speciation and peripheral isolation have uncertain importance in species accumulation, and are largely overshadowed by assumed dominance of allopatric modes of speciation. Understanding the role of different speciation mechanisms within biodiversity hotspots is central to understanding the generation of biological diversity. Here, we use a phylogeographic analysis of the spiny-throated reed frogs and examine sister pairings with unbalanced current distributional ranges for characteristics of peripatric speciation. We further investigate whether forest/grassland mosaic adapted species are more likely created through peripatric speciation due to instability of this habitat type. RESULTS: We reconstructed a multi-locus molecular phylogeny of spiny-throated reed frogs which we then combined with comparative morphologic data to delimit species and analyze historical demographic change; identifying three new species. Three potential peripatric speciation events were identified along with one case of allopatric speciation. Peripatric speciation is supported through uneven potential and realized distributions and uneven population size estimates based on field collections. An associated climate shift was observed in most potentially peripatric splits. Morphological variation was highest in sexually dimorphic traits such as body size and gular shape, but this variation was not limited to peripatric species pairs as hypothesized. The potentially allopatric species pair showed no niche shifts and equivalent effective population sizes, ruling out peripatry in that speciation event. Two major ecological niche shifts were recovered within this radiation, possibly as adaptations to occupy areas of grassland that became more prevalent in the last 5 million years. Restricted and fluctuating grassland mosaics within forests might promote peripatric speciation in the Eastern Arc Biodiversity Hotspot (EABH). CONCLUSIONS: In our case study, peripatric speciation appears to be an important driver of diversity within the EABH biodiversity hotspot, implying it could be a significant speciation mechanism in highly fragmented ecosystems. Extensive peripatric speciation in this montane archipelago may explain the abundance of discrete lineages within the limited area of the EABH, as inferred in remote island archipelagos. Future phylogenetic studies incorporating demographic and spatial analyses will clarify the role of peripatric speciation in creating biodiversity hotspots.