Unlocking the vault: next-generation museum population genomics.

Natural history museum collections provide unique resources for understanding how species respond to environmental change, including the abrupt, anthropogenic climate change of the past century. Ideally, researchers would conduct genome-scale screening of museum specimens to explore the evolutionary consequences of environmental changes, but to date such analyses have been severely limited by the numerous challenges of working with the highly degraded DNA typical of historic samples. Here, we circumvent these challenges by using custom, multiplexed, exon capture to enrich and sequence ~11,000 exons (~4 Mb) from early 20th-century museum skins. We used this approach to test for changes in genomic diversity accompanying a climate-related range retraction in the alpine chipmunks (Tamias alpinus) in the high Sierra Nevada area of California, USA. We developed robust bioinformatic pipelines that rigorously detect and filter out base misincorporations in DNA derived from skins, most of which likely resulted from postmortem damage. Furthermore, to accommodate genotyping uncertainties associated with low-medium coverage data, we applied a recently developed probabilistic method to call single-nucleotide polymorphisms and estimate allele frequencies and the joint site frequency spectrum. Our results show increased genetic subdivision following range retraction, but no change in overall genetic diversity at either nonsynonymous or synonymous sites. This case study showcases the advantages of integrating emerging genomic and statistical tools in museum collection-based population genomic applications. Such technical advances greatly enhance the value of museum collections, even where a pre-existing reference is lacking and points to a broad range of potential applications in evolutionary and conservation biology.

Comment and integration to Andreone et al. 2022 "Reconnecting research and natural history museums in Italy and the need of a national collection biorepository".

In Andreone et al. (2022), the authors described a background about the Italian Natural History Museums (NHMs) situation, highlighting difficulties regarding the coordination among institutes due to the fragmented landscape, from the past until today. They suggested how having a national institute, the Future National Biodiversity Centre (FCNB), woul d represent the best solution to the problem. Our vision regarding the lack of a national natural history museum in Italy does not coincide with that of the authors, but we do not consider clarifying this aspect in the present letter. On the other hand, since the authors reported how "the present fragmentation of museums and associated collections does not allow for an effective participation of Italy to global models of aggregated natural history databases (such as the VertNet, iDigBio, GBIF)", we believe it is necessary to address the issue linked to the digital sharing of Italian collections. We present more clarifications about Italy's commitment to the digitisation and sharing of NH collections data through the DiSSCo RI "Distributed System of Scientific Collections Research Infrastructure" of which Italy is one of the 23 European partner countries since 2018.

Historical museum collections and contemporary population studies implicate roads and introduced predatory bullfrogs in the decline of western pond turtles.

The western pond turtle (WPT), recently separated into two paripatrically distributed species (Emys pallida and Emys marmorata), is experiencing significant reductions in its range and population size. In addition to habitat loss, two potential causes of decline are female-biased road mortality and high juvenile mortality from non-native predatory bullfrogs (Rana catesbeiana). However, quantitative analyses of these threats have never been conducted for either species of WPT. We used a combination of historical museum samples and published and unpublished field studies shared with us through personal communications with WPT field researchers (B. Shaffer, P. Scott, R. Fisher, C. Brown, R. Dagit, L. Patterson, T. Engstrom, 2019, personal communications) to quantify the effect of roads and bullfrogs on WPT populations along the west coast of the United States. Both species of WPT shift toward increasingly male biased museum collections over the last century, a trend consistent with increasing, female-biased road mortality. Recent WPT population studies revealed that road density and proximity were significantly associated with increasingly male-biased sex ratios, further suggesting female-biased road mortality. The mean body size of museum collections of E. marmorata, but not E. pallida, has increased over the last 100 years, consistent with reduced recruitment and aging populations that could be driven by invasive predators. Contemporary WPT population sites that co-occur with bullfrogs had significantly greater average body sizes than population sites without bullfrogs, suggesting strong bullfrog predation on small WPT hatchlings and juveniles. Overall, our findings indicate that both species of WPT face demographic challenges which would have been difficult to document without the use of both historical data from natural history collections and contemporary demographic field data. Although correlational, our analyses suggest that female-biased road mortality and predation on small turtles by non-native bullfrogs are occurring, and that conservation strategies reducing both may be important for WPT recovery.

Assessing migration patterns in Passerina ciris using the world's bird collections as an aggregated resource.

Natural history museum collections (NHCs) represent a rich and largely untapped source of data on demography and population movements. NHC specimen records can be corrected to a crude measure of collecting effort and reflect relative population densities with a method known as abundance indices. We plotted abundance index values from georeferenced NHC data in a 12-month series for the new world migratory passerine Passerina ciris across its molting and wintering range in Mexico and Central America. We illustrated a statistically significant change in abundance index values across regions and months that suggests a quasi-circular movement around its non-breeding range, and used enhanced vegetation index (EVI) analysis of remote sensing plots to demonstrate non-random association of specimen record abundance with areas of high primary productivity. We demonstrated how abundance indices from NHC specimen records can be applied to infer previously unknown migratory behavior, and be integrated with remote sensing data to provide a deeper understanding of demography and behavioral ecology across time and space.