Historical Specimens Research Articles

A phylogenomic tree of wood-warblers (Aves: Parulidae): Dealing with good, bad, and ugly samples.

The New World warblers (Parulidae) are a model group for ecological and evolutionary analyses. However, current phylogenetic relationships across this family are based upon few loci. Here we use ultraconserved elements (UCEs) to estimate a rigorous species-level phylogeny for the family. As is true for many groups, high-quality tissues were unavailable for some taxa. Thus, we explored methods for incorporating sequences derived from historical (toe pad) samples to expand the phylogenetic datasets. We recovered an average of 4,186 UCE loci and mitochondrial bycatch data (supplemented with published mitochondrial data) from 96 % of all currently recognized species. We found that the UCE phylogeny built with alignments with less than 70 % of gaps and ambiguities recovered the most robust phylogenetic relationships for this family, representing 101 species. Using this phylogeny as a topological backbone and adding ten fair quality "bad" samples effectively generated an overall well supported phylogeny, representing 108 species (∼90 % of all species). Based on this tree, we then added in seven poor quality "ugly" samples and six of those were placed within their expected genera. We also explored the phylogenetic positions of the likely extinct Leucopeza semperi and the endangered Catharopeza bishopi where limited data was obtained. Overall, taxonomic placements in our UCE trees largely correspond to previously published studies with the recovery of all currently recognized genera as monophyletic except for Basileuterus which was rendered paraphyletic by B. lachrymosus. Our study provides insights in understanding the phylogenetic relationships of a model Passeriformes family and outlines effective practices for managing sparse genomic data sourced from historical museum specimens. Variable topological arrangements across datasets and analyses reflect the evolutionary complexity of this group and provide future topics for in-depth studies.

Revised taxonomy of Synodontis catfishes (Siluriformes: Mochokidae) from the Lake Tanganyika basin reveals lower species diversity than expected

Abstract Synodontis Cuvier, 1816 is a species-rich group of African catfishes. Prior to this analysis, 13 species of Synodontis were recognized from Lake Tanganyika and its tributaries, composing the only extant lacustrine radiation of the genus, with a unique origin of obligate brood parasitism among all fishes. Species differentiation and phylogenetic relationships of this group remained largely unresolved. Herein, the taxonomy of Synodontis in the Lake Tanganyika basin is revised, including redescriptions of all species and an updated identification key. Genetic (mitochondrial and nuclear genomic markers) and morphological data suggest a lower species diversity than previously recognized, supporting the distinction of 10 Synodontis species in the lake basin. Based on our findings, we recognize Synodontis grandiops, Synodontis ilebrevis, and Synodontis lucipinnis as junior synonyms of Synodontis multipunctatus, Synodontis polli, and Synodontis petricola, respectively. No recent material of Synodontis dhonti and Synodontis tanganyicae (with Synodontis lacustricolus as a synonym) was available. Morphometric/meristic data suggest their close relationship to Synodontis granulosus. Sequencing of historical specimens inferred S. tanganyicae as sister to S. granulosus but with a 1.7% divergence based on mitochondrial data. In contrast to previous studies, phylogenomic data support the lacustrine assemblage of Synodontis in Lake Tanganyika as monophyletic.

A Genomic Exploration of the Possible De-Extirpation of the Zanzibar Leopard.

The recently extirpated Zanzibar leopard was the only known African leopard (Panthera pardus spp.) population restricted exclusively to a major island habitat. Although its demise was driven through habitat change and conflict with humans, given its role as a keystone species for the Zanzibar Archipelago, its successful potential reintroduction might offer a means for helping preserve the natural biodiversity of its former habitat. Whether this is feasible, however, would be contingent on both whether closely related source populations can be identified on mainland Africa, and whether the Zanzibar form exhibited any special adaptations that might need to be considered when choosing such a source. In light of these questions, we genomically profiled two of the six known historic specimens, to explore whether they represent a realistic candidate for de-extirpation through reintroduction. Our analyses indicate that despite its geographical separation, the Zanzibar leopard shared a close genetic relationship with mainland East African individuals. Furthermore, although its uniqueness as an island population was emphasised by genomic signatures of high inbreeding and increased mutation load, the latter similar to the level of the critically endangered Amur leopard (P. p. orientalis), we find no evidence of functionally significant genetic diversity unique to Zanzibar. We therefore conclude that should attempts to restore leopards to Zanzibar be considered, then mainland East African leopards would provide a suitable gene pool.

Performance of historical ferrocement specimens subjected to corrosive environments

AbstractFerrocement is a type of thin wall‐reinforced concrete composed of hydraulic cement mortar reinforced with several layers of steel wire mesh. The material is used as a low‐cost construction and retrofit solution and allows the creation of very thin elements. In the past, the material was also used to build some structural engineering masterpieces that currently face preservation challenges. Despite the use of the material, few studies have analyzed its durability with respect to corrosion and its evaluation for preservation purposes. The paper presents the results of a testing campaign on ferrocement replica specimens subjected to a corrosive environment. After an aggressive aging procedure, where the specimens are exposed to chloride ingress, the specimens are tested through a four‐point bending test to compare their performances. Results of the mechanical behavior are compared to the results from the half‐cell potential monitoring carried out during the aging process and optical microscope acquisitions regarding the cross‐sectional corrosion‐loss area in the wires. The aim is to assess the performance of historical ferrocement exposed to degradation due to corrosion; this can be useful in identifying the best procedures to protect and preserve it, as well as in evaluating its performance over time.

A Snakemake Toolkit for the Batch Assembly, Annotationand Phylogenetic Analysis of Mitochondrial Genomes and Ribosomal Genes From Genome Skims of Museum Collections.

Low coverage 'genome-skims' are often used to assemble organelle genomes and ribosomal gene sequences for cost-effective phylogenetic and barcoding studies. Natural history collections hold invaluable biological information, yet poor preservation resulting in degraded DNA often hinders polymerase chain reaction-based analyses. However, it is possible to generate libraries and sequence the short fragments typical of degraded DNA to generate genome-skims from museum collections. Here we introduce a snakemake toolkit comprised of three pipelines skim2mito, skim2rrna and gene2phylo, designed to unlock the genomic potential of historical museum specimens using genome skimming. Specifically, skim2mito and skim2rrna perform the batch assembly, annotation and phylogenetic analysis of mitochondrial genomes and nuclear ribosomal genes, respectively, from low-coverage genome skims. The third pipeline gene2phylo takes a set of gene alignments and performs phylogenetic analysis of individual genes, partitioned analysis of concatenated alignments and a phylogenetic analysis based on gene trees. We benchmark our pipelines with simulated data, followed by testing with a novel genome skimming dataset from both recent and historical solariellid gastropod samples. We show that the toolkit can recover mitochondrial and ribosomal genes from poorly preserved museum specimens of the gastropod family Solariellidae, and the phylogenetic analysis is consistent with our current understanding of taxonomic relationships. The generation of bioinformatic pipelines that facilitate processing large quantities of sequence data from the vast repository of specimens held in natural history museum collections will greatly aid species discovery and exploration of biodiversity over time, ultimately aiding conservation efforts in the face of a changing planet.

The Euphorbia bivonae aggregate (Euphorbiaceae) in the Central Mediterranean area: First report of Euphorbia papillaris from Tunisia

During floristic field exploration within the Tunisian territory, an interesting Euphorbia population was sampled from the Haouaria region in Cap-Bon peninsula. After critical study of the collected specimens against closely related taxa of the Euphorbia bivonae aggregate and following review of relevant literature and herbarium specimens, that population was identified as E. papillaris. This species is very rare and was considered endemic to western Sicily. The revision of historical herbarium specimens in the main European herbaria led to document the occurrence of this species also in Libya. An updated geographical distribution for the E. bivonae aggregate in the Central Mediterranean area as well as floristic and ecological data are here provided. An identification key is also presented.

First record of <i>Abrothrix olivacea</i> (Waterhouse, 1837) in Peru based on historical material from Tacna

Abrotrichini is the sigmodontine tribe with the fewest species in Peru, known only from two species: Abrothrix andina and Ab. jelskii, both distributed in the high Andean regions of Peru above 3000 m in altitude. A detailed review of the morphology of historical specimens collected in the Tacna department and identified as Akodon mollis was conducted. As a result, we found that the examined specimens corresponded to Abrothrix olivacea, a species previously known only from Chile and Argentina. This discovery represents the first record of this species in Peru, extending its distribution range 165 km north of its previous northernmost record in Quebrada Camarones, Arica-Parinacota, Chile. Furthermore, this finding significantly reduces the distribution range of Akodon mollis to the northwestern region of Peru. We also provide key craniodental characters to differentiate species of Abrothrix and Akodon in southwestern Peru and northern Chile. For Peru, this record increases the diversity of mammals to 588 species and rodents to 201 species. In the case of the Tacna department, mammalian diversity increases to 47 species. This work highlights the value of natural history museum collections in enhancing our understanding of species diversity.

An overview of the Brazilian Atlantic Forest species of Pachythone Bates (Lepidoptera: Riodinidae), with the description of a new species and an updated checklist of Pachythonina

The taxonomy of the Brazilian Atlantic Forest endemic species belonging to the Neotropical metalmark genus Pachythone Bates, 1868 is revised. A new endemic species is described, Pachythone gagarini Dolibaina & Dias, sp. nov., based on historical specimens from a single locality in Rio de Janeiro state. Adults and genitalia of the new species are illustrated and described in detail. Pachythone palades Hewitson, (1873) and P. pasicles Hewitson, (1873), described from females and males, respectively, and regarded as two distinct species since their descriptions, are here recognized as a single species, the former being considered a junior subjective synonym of the latter (syn. nov.). Lectotypes are designated for both P. palades and P. pasicles. Pachythone sumare Callaghan, 1999, so far known from its type locality in Rio de Janeiro state, is here reported from Joinville, Santa Catarina, which extends its occurrence 700 km southwards. Lastly, an updated checklist for the recently proposed subtribe Pachythonina is given.

Genomics of historical museum collections clarifies species diversity in Cuban hutias (Capromys)

Abstract Specimen-based taxonomic research is essential for understanding diversity and setting management frameworks for threatened mammal faunas, and ancient DNA techniques are increasingly used to extract information from taxonomically relevant historical specimens. The largest survivors of the depleted Caribbean mammal fauna are hutias in the genus Capromys, which is usually interpreted as containing a single species, C. pilorides. Previous studies have demonstrated genetic differentiation of Capromys populations across Cuba, but infrageneric species diversity and nomenclature remain unclear. We conducted ancient DNA analysis of historical Capromys samples using cytochrome b and complete mitogenome data sets, and including the 19th-century holotypes of 2 species now considered synonyms, C. fournieri and C. geayi. Our analyses identify distinct western and central/eastern Capromys clades that diverged 1.75 Mya based upon mitogenome data. These clades are separated by the Havana–Matanzas Channel, which represented a barrier to dispersal throughout the Neogene–Quaternary. Divergence date comparisons with other hutia species provide support for interpreting divergence between Capromys populations as species-level differentiation. Although we were unable to yield amplifiable DNA from the C. fournieri holotype, our analyses confidently assign the C. geayi holotype to the western Capromys clade. We therefore recognize 2 extant Capromys species: C. geayi (western Cuba) and C. pilorides (central/eastern Cuba and Cayman Islands).

Museum specimens shedding light on the evolutionary history and cryptic diversity of the hedgehog family Erinaceidae.

The family Erinaceidae encompasses 27 extant species in two subfamilies: Erinaceinae, which includes spiny hedgehogs, and Galericinae, which comprises silky-furred gymnures and moonrats. Although they are commonly recognized by the general public, their phylogenetic history remains incompletely understood, and several species have never been included in any molecular analyses. Additionally, previous research suggested that the species diversity of Erinaceidae might be underestimated. In this study, we sequenced the mitochondrial genomes of 29 individuals representing 18 erinaceid species using 18 freshly collected tissue and 11 historical museum specimens. We also integrated previously published data for a concatenated analysis. We aimed to elucidate the evolutionary relationships within Erinaceidae, estimate divergence times, and uncover potential underestimated species diversity. Our data finely resolved intergeneric and interspecific relationships and presented the first molecular evidence for the phylogenetic position of Mesechinus wangi, Paraechinus micropus, and P. nudiventris. Our results revealed a sister relationship between Neotetracus and Neohylomys gymnures, as well as a sister relationship between Hemiechinus and Mesechinus, supporting previous hypotheses. Additionally, our findings provided a novel phylogenetic position for Paraechinus aethiopicus, placing it in a basal position within the genus. Furthermore, our study uncovered cryptic species diversity within Hylomys suillus as well as in Neotetracus sinensis, Atelerix albiventris, P. aethiopicus, and Hemiechinus auratus, most of which have been previously overlooked.

The evolutionary history of wild and domestic brown rats (Rattus norvegicus).

The brown rat (Rattus norvegicus) occupies nearly every terrestrial habitat with a human presence and is one of our most important model organisms. Despite this prevalence, gaps remain in understanding the evolution of brown rat commensalism, their global dispersal, and mechanisms underlying contemporary adaptations to diverse environments. In this Review, we explore recent advances in the evolutionary history of brown rats and discuss key challenges, including finding and accurately dating historical specimens, disentangling histories of multiple domestication events, and synthesizing functional variation in wild rat populations with the development of laboratory strains. Advances in zooarchaeology and population genomics will usher in a new golden age of research on the evolutionary biology of brown rats, with positive feedbacks on their use as biomedical models.

Untangling the colonization history of the Australo-Pacific reed warblers, one of the world's great island radiations.

Island radiations, such as those of the Australo-Pacific, offer unique insight into diversification, extinction, and early speciation processes. Yet, their speciation and colonization histories are often obscured by conflicting genomic signals from incomplete lineage sorting or hybridization. Here, we integrated mitogenomes and genome-wide SNPs to unravel the evolutionary history of one of the world's most geographically widespread island radiations. The Australo-Pacific reed warblers (Acrocephalus luscinius complex) are a speciose lineage including five species that have become extinct since the 19th century and ten additional species of conservation concern. The radiation spans over 10,000 km across Australo-Papua, Micronesia and Polynesia, including the Mariana, Hawaii and Pitcairn Island archipelagos. Earlier mtDNA studies suggested a stepping-stone colonization process, resulting in archipelago-level secondary sympatry of divergent mtDNA lineages in the Mariana Islands and Marquesas. These studies hypothesised that morphologically similar species on neighbouring islands arose from ecological convergence. Using hDNA from historical museum specimens and modern genetic samples, we show that incomplete lineage sorting and/or gene flow have shaped the radiation of Australo-Pacific reed warblers rather than secondary sympatry. The nuclear genome reconstructs a simpler biogeographic history than mtDNA, showing close relationships between species in the Mariana Islands and Marquesas despite their paraphyletic mtDNA lineages. Gene flow likely involved early and late colonizing waves of the radiation before the loss of ancestral dispersive ability. Our results highlight how collection genomics can elucidate evolutionary history and inform conservation efforts for threatened species.

Restoring a natural skeleton of a premature infant from the early twentieth century

Traditional anatomical preparations as they are often found in university collections are both historical treasure and moral responsibility of the hosting institutions. These remains not only represent the tradition and history of anatomical science and education, but above all are the remains of human beings and thus should be treated with dignity. While the discussion on public display of historical human remains is ongoing, the responsibility to keep them in an optimal state of preservation is not in question. However, most time-honored anatomical collections do or did not have the financial and/or technical capacity to keep these high standards, underlining the need for exchange of technical know-how between anatomical institutes and the support of restoration/conservation professionals. Here, we present a state-of-the-art conservation and restoration of a fetal natural skeleton from the early twentieth century along with the professional documentation of restoration-measures. Therefore, we used modern photo- and video documentation, including photogrammetry, as well as UV- and x-ray-examinations to record historical and new restoration procedures. We carried out measures to reconstitute the structural stability of the skeleton. Moreover, we replaced lost parts of the left foot skeleton, and critically discuss the legitimacy of body part replacement in historical specimens. We are convinced, that similar cases of insufficiently preserved specimens can be found in most anatomical collections. Therefore, this article is not only intended to document the state-of-the-art conservation and restoration of a natural skeleton, but also serve as an inspiration for similar campaigns in other institutions in the future.

Urbanization-associated range expansion genetically homogenizes a butterfly species

Human-induced environmental change and globalization facilitate biological invasions, which can lead to the displacement of native species by non-native ones.1,2,3,4 Analogously, biodiversity loss may occur within species when habitat modifications facilitate the expansion of a specific population's range, leading to genetic admixture with native local populations. We demonstrate such intraspecific loss in population-level diversity in the Southern Small White (Pieris mannii), an originally sedentary butterfly5 that recently expanded its range across Central Europe due to urbanization.6,7,8 Using genome-wide markers from historical museum specimens and contemporary samples, we identify a distinct population initiating this expansion and reveal the genetic homogenization of native local populations by admixture with the expansive one. Our study illustrates how human-made environmental change can simultaneously benefit a species by permitting range expansion and drive cryptic biodiversity loss through the genetic homogenization of conspecific populations.

Recovering plant-associated arthropod communities by eDNA metabarcoding historical herbarium specimens

Natural history collections are a priceless resource for understanding patterns and processes of biodiversity change in the Anthropocene.1 Herbaria, which house millions of historical plant records from all over the globe, are particularly valuable to study population genetics of the plants themselves and to understand the assembly of plant-associated microbial communities.2 Here we test if herbaria can serve yet another essential purpose, namely to provide information on the historical assembly of plant-arthropod interactions. The specificity and temporal stability of these associations are poorly known.3 Considering their pivotal role in the assembly of terrestrial food webs,4 this knowledge is paramount to understanding the consequences of global change. We use environmental DNA (eDNA) metabarcoding to characterize communities of plant-associated arthropods from archived herbarium specimens of different ages and origins. The herbarium specimens yield arthropod DNA across various ecological guilds and trophic levels over multiple decades. In an experiment, we also show that the typical dry storage of plants in herbaria does not alter the recovered arthropod diversity and community composition. By analyzing a time series of leaf samples from a forest monitoring project, we then characterize changes in arthropod biodiversity over two decades, showing that archived plants can also provide the time series data that are urgently needed to understand arthropod declines.5 This use of herbaria and plant archives promises unprecedented insights into plant-arthropod interactions and revolutionizes our ability to monitor spatiotemporal changes in interaction diversity.

Herbaria: a valuable resource of the time treasured historic plant specimens with boundless research potential for environmental sustainability

Herbaria: a valuable resource of the time treasured historic plant specimens with boundless research potential for environmental sustainability

Century-long timelines of herbarium genomes predict plant stomatal response to climate change

Dissecting plant responses to the environment is key to understanding whether and how plants adapt to anthropogenic climate change. Stomata, plants’ pores for gas exchange, are expected to decrease in density following increased CO2 concentrations, a trend already observed in multiple plant species. However, it is unclear whether such responses are based on genetic changes and evolutionary adaptation. Here we make use of extensive knowledge of 43 genes in the stomatal development pathway and newly generated genome information of 191 Arabidopsis thaliana historical herbarium specimens collected over 193 years to directly link genetic variation with climate change. While we find that the essential transcription factors SPCH, MUTE and FAMA, central to stomatal development, are under strong evolutionary constraints, several regulators of stomatal development show signs of local adaptation in contemporary samples from different geographic regions. We then develop a functional score based on known effects of gene knock-out on stomatal development that recovers a classic pattern of stomatal density decrease over the past centuries, suggesting a genetic component contributing to this change. This approach combining historical genomics with functional experimental knowledge could allow further investigations of how different, even in historical samples unmeasurable, cellular plant phenotypes may have already responded to climate change through adaptive evolution.

Rediscovering the unusual Cancellus makrothrix Stebbing, 1924 (Crustacea: Decapoda: Diogenidae) in the “Great African Seaforest”

The rare diogenid hermit crab Cancellus makrothrix Stebbing, 1924, previously known from only a few specimens collected a century ago from Algoa Bay, South Africa, has been found to be common in the kelp forest known as the “Great African Seaforest”, and rocky reefs, of False Bay, South Africa. This poorly known species, considered “aberrant” by some carcinologists, is one of 17 known in the genus Cancellus H. Milne Edwards, 1836, and the only of the genus known to occur in the coast of southern Africa. Cancelllus makrothrix lives in gastropod shells, whereas all other congenerics live in a variety of petricolous dwellings that are either excavated or worn away into cylindrical cavities. The newly collected material of C. makrothrix in South Africa, together with the study of historical museum specimens has made possible the detailed redescription and taxonomic discussion of this species presented herein, using full illustrations, photographs, and microCT scans. For future reference, the molecular CO1 genetic barcode is reported. A lectotype is selected from Stebbing’s original syntype material found to consist of two specimens: a female of which only several appendages remain, in the Natural History Museum, London, and a male, illustrated in the original description, in the Iziko South African Museum, Cape Town. Taxonomic remarks, comments on biological oddities, brief in situ and laboratory observations of live specimens, and a map summarizing the world distribution of species of Cancellus, are included.

Ten new species and notes on the genus Psoralea L. (Psoraleeae, Fabaceae) from South Africa

Background and aims – Following detailed phylogenetic and biogeographic studies of the tribe Psoraleeae, the genus Psoralea L. was shown to have been derived out of Otholobium C.H.Stirt. As Psoralea has nomenclatural priority, Otholobium has been subsumed into Psoralea, whereby two broad subgeneric groups are aligned with the previous descriptions of the separate genera, but some problems of placement of a few species remain unresolved. Work is ongoing to study and describe the nearly 20 undescribed species that will have to be considered before sectional groups can be established. In this paper we describe ten new species, including several putative taxa already recognized in regional floras, based on historic specimens and more recent field collections. Material and methods – Standard practices of herbarium and field taxonomy have been applied to study herbarium material available at B, BLFU, BM, BOL, BR, E, GRA, J, JRAU, K, KEI, L, LE, LINN, M, MO, NBG, NH, NU, NY, OXF, P, PRA, PRC, PRE, PRU, S, SAM, SCHG, SRGH, TCD, Z, ZT, and US. Additional material was provided from fieldwork by the authors and collaborators. Key results – Ten new species of Psoralea from southern Africa are described: Psoralea crista C.H.Stirt. & Muasya, P. fulva C.H.Stirt. & Muasya, P. luteovirens C.H.Stirt. & Muasya, P. nubicola C.H.Stirt. & Muasya, P. oreopola C.H.Stirt., P. pallescens C.H.Stirt. & Muasya, P. papillosa C.H.Stirt. & Muasya, P. prompta C.H.Stirt. & Muasya, P. schutteae C.H.Stirt. & Muasya, and P. vlokii C.H.Stirt. & Muasya. Conclusion – The newly described species, all restricted to South Africa, increases the number of Psoralea species to 129. These species arise from expanded fieldwork into previously under-collected areas, as well as from better refinement in species delimitations in the leafless ‘aphylla’ and pinnately-leaved species complexes.

Effects of pre-treatment, historical age, and sample characteristics on the stable isotope analyses of killer whale (Orcinus orca) bone.

Stable isotope analysis of bone provides insight into animal foraging and allows for ecological reconstructions over time, however pre-treatment is required to isolate collagen. Pre-treatments typically consist of demineralization to remove inorganic components and/or lipid extraction to remove fats, but these protocols can differentially affect stable carbon (δ13C) and nitrogen (δ15N) isotope values depending on the chemicals, tissues, and/or species involved. Species-specific methodologies create a standard for comparability across studies and enhance understanding of collagen isolation from modern cetacean bone. Elemental analyzers coupled to isotope ratio mass spectrometers were used to measure the δ13C and δ15N values of powdered killer whale (Orcinus orca) bone that was intact (control) or subjected to one of three experimental conditions: demineralized, lipid-extracted, and both demineralized and lipid-extracted. Additionally, C:N ratios were evaluated as a proxy for collagen purity. Lastly, correlations were examined between control C:N ratios vs. historical age and control C:N ratios vs. sample characteristics. No significant differences in the δ15N values were observed for any of the experimental protocols. However, the δ13C values were significantly increased by all three experimental protocols: demineralization, lipid extraction, and both treatments combined. The most influential protocol was both demineralization and lipid extraction. Measures of the C:N ratios were also significantly lowered by demineralization and both treatments combined, indicating the material was closer to pure collagen after the treatments. Collagen purity as indicated via C:N ratio was not correlated with historical age nor sample characteristics. If only the δ15N values from killer whale bone are of interest for analysis, no pre-treatment seems necessary. If the δ13C values are of interest, samples should be both demineralized and lipid-extracted. As historical age and specimen characteristics are not correlated with sample contamination, all samples can be treated equally.