Museomics of Carabus giant ground beetles shows an Oligocene origin and in situ alpine diversification
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Abstract
The development of museomics represents a major paradigm shift in the use of natural history collection specimens for systematics and evolutionary biology. New approaches in this field allow the sequencing of hundreds to thousands of loci from across the genome using historical DNA. HyRAD-X, a recently introduced capture method using bench-top designed probes, has proved very efficient for recovering genomic-scale datasets using natural history collection specimens. Using this technique at both the intra- and interspecific levels, we infer the most robust phylogeny to date for Arcifera, an ecologically and morphologically diverse clade of Carabus giant ground beetles. We successfully generated a genomic dataset of up to 1965 HyRAD-X loci for all described species, permitting inference of a robust dated phylogenomic tree for this clade. Our species delimitation and population genomic analyses suggest that the current classification for Arcifera is in line with its evolutionary history. Our results suggest an origin of Arcifera in the late Oligocene followed by speciation events during the warm mid-Miocene unlinked to Pleistocene glaciations. The dynamic paleogeographic history of the Palearctic region likely contributed to the diversification of this lineage with a relatively ancient colonization of the proto-Alps followed by in situ speciation where most species of Arcifera are currently found sometimes syntopically likely as a result of post-glaciations secondary contacts.
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Some of the biodiversity of our planet now exists only in museums, due to continuing habitat destruction and climate change. With more than 380 million entomological specimens already preserved in museums (Johnson and Owens 2023), there is much work left to document what we already have. Fortunately, new advances in DNA sequencing have given us the opportunity to get enormous amounts of information from dried specimens on pins.
One such advance is HyRAD-X, which uses RAD-derived probes originally developed using RNA extracted from a selection of specimens with high RNA-integrity (Schmid et al. 2017). These exome-limited probes can then be used to capture low-integrity DNA extracted from a single leg from museum specimens, followed by Illumina sequencing of the enriched libraries.
Ground beetles allow an excellent demonstration of this …Some of the biodiversity of our planet now exists only in museums, due to continuing habitat destruction and climate change. With more than 380 million entomological specimens already preserved in museums (Johnson and Owens 2023), there is much work left to document what we already have. Fortunately, new advances in DNA sequencing have given us the opportunity to get enormous amounts of information from dried specimens on pins.
One such advance is HyRAD-X, which uses RAD-derived probes originally developed using RNA extracted from a selection of specimens with high RNA-integrity (Schmid et al. 2017). These exome-limited probes can then be used to capture low-integrity DNA extracted from a single leg from museum specimens, followed by Illumina sequencing of the enriched libraries.
Ground beetles allow an excellent demonstration of this approach, as their diversity, large size, and charismatic appearance has led to them being well represented in museums. Using a HyRAD-X probe set previously developed for a higher phylogeny within the subfamily Carabinae (Toussaint et al. 2021), the authors have now applied the same probe set to produce a comprehensive phylogeny for Arcifera, a clade of four subgenera and ten species within the genus Carabus (Pauli et al. 2024).
Of the 96 specimens that they started out with, 90% were from natural history collections and 40% dropped out immediately due to poor DNA extraction yield. After filtering the resulting sequence reads for minimum coverage and minimum number of samples per locus, they ended up with 35 museum specimens with an average of 793 loci. Phylogenetic analysis of this data supported the current classification of these beetles.
Pauli et al’s. (2024) study has effectively shown the power of HyRAD-X methods for applications at the species level. In-house production of probes makes the method accessible, expanding the opportunity to use museum specimens for population genetic research.
ReferencesJohnson KR, Owens, (IFP. 2023) A global approach for natural history museum collections. Science 379,1192-1194(2023). https://doi.org/10.1126/science.adf6434
Pauli MT, Gauthier J, Labédan M, Blanc M, Bilat J, Toussaint EFA (2024) Museomics of Carabus giant ground beetles shows an Oligocene origin and in situ alpine diversification. bioRxiv, ver. 5 peer-reviewed and recommended by Peer Community in Zoology. https://doi.org/10.1101/2024.03.21.586057
Schmid, S., Genevest, R., Gobet, E., Suchan, T., Sperisen, C., Tinner, W. and Alvarez, N. (2017), HyRAD-X, a versatile method combining exome capture and RAD sequencing to extract genomic information from ancient DNA. Methods Ecol Evol, 8: 1374-1388. https://doi.org/10.1111/2041-210X.12785
Toussaint EFA, Gauthier J, Bilat J, Gillett CPDT, Gough HM, Lundkvist H, Blanc M, Muñoz-Ramírez CP, Alvarez N (2021) HyRAD-X Exome Capture Museomics Unravels Giant Ground Beetle Evolution, Genome Biology and Evolution, Volume 13, Issue 7, evab112, https://doi.org/10.1093/gbe/evab112
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