Night at the museum

Many population genetic and genomic studies document snapshots of a given population’s genetic diversity. Yet, there are many reasons to document changes over time in population parameters in response to perturbations, such as biological invasions (both in terms of the invader and the invaded).
There is a rich history of long-term ecological monitoring in which the abundance and distribution of species are recorded. For example, the MarClim project has continued efforts by the Marine Biological Association of the United Kingdom of monitoring intertidal zones, in which records date back to the 1950s. However, these monitoring projects tend to be concerned with ecological patterns rather than documenting genetic change through time.

Extension of the leading range edges occurring in the Lusitanian species Perforatus perforatus, Phorcus lineatus, Gibbula umbilicalis, Chthamalus stellatus, Bifurcaria, and then contractions of the southern trailing range edge of the Boreal species Alaria esculenta and Semibalanus balanoides. © Nova Mieszkowska

Extension of the leading range edges occurring in the Lusitanian species Perforatus perforatus, Phorcus lineatus, Gibbula umbilicalis, Chthamalus stellatus, Bifurcaria bifurcata, and then contractions of the southern trailing range edge of the Boreal species Alaria esculenta and Semibalanus balanoides. © Nova Mieszkowska


There are studies in which genetic change through time has been studied, such as Reem et al. (2013) in which limited gene flow associated with high mutation rates was documented in the ascidian Botryllus schlosseri over a 13-year period. But, what about larger scales, both spatial and temporal?

Silvertown et al. (2006) reviewed the Park Grass Experiment, begun in 1856. It is a unique example of ecological research both in terms of its longevity, but also the diversity of empirical research over the past 150 years.
The Park Grass experiment at Rothamsted. © Rothamsted Research

The Park Grass experiment at Rothamsted. © Rothamsted Research


The archive of hay samples from Park Grass contains material from multiple populations that have since gone extinct. It would, therefore, be possible to retrospectively analyze the genetic composition of recorded extinctions.
Outside of these long-term experiments, are there other repositories? Can we, as molecular ecologists, travel through time at our benches?
By sifting through museum collections and herbaria that cover broad array of taxonomic groups, we can. Certainly, the importance of museum specimens for taxonomic and phylogenetic purposes has long been noted (e.g., Shapiro et al. 2002), but museums and natural history collections have an underutilized population genetic resource.
A herbarium specimen of the non-native seaweed Grateloupia turuturu from the Natural History Museum London © S.A. Krueger-Hadfield

A herbarium specimen of the seaweed Grateloupia turuturu from the collection housed at the Natural History Museum London © S.A. Krueger-Hadfield


Wandeler, Hoeck and Keller (2007) provided one of the first reviews of the use of museum specimens in population genetics. They summarized the types of analyses (e.g., changes in genetic diversity, effective population size, changes in connectivity and detecting introductions and introgression), potential pitfalls and future prospects for material tucked away in museums, herbaria and private collections.
Out of 382 studies documented by Lavoie (2013) to have utilized herbarium material, only 17 employed molecular analyses.
One of the first studies, by Provan et al. (2007), exploited algal herbarium specimens and was able to identify cryptic invasions of the green alga Codium fragile.  These invasions have been occurring for much longer than records indicated. In some cases, nearly 100 years had elapsed from the arrival of the invasive tomentosoides strain until it was noticed.
In 2014, Martin et al. used herbarium specimens (> 400 herbarium specimens; date of sampling ranged between 1873 to 1939 with median year of 1914) and natural populations (464 plants from 45 wild populations) of common ragweed (Ambrosia artemisiifolia ). The authors attribute the shift in spatial boundaries detected using historical and modern datasets with:

seed-mediated gene flow associated with agricultural disturbance during westward expansion of human populations from the Atlantic Coast.

Dormontt et al. (2014) demonstrated the:

utility of molecular studies of contemporary and historical field collections [in Senecio madagascariensis. These datasets] can be combined to reconstruct a more complete picture of the invasion history of introduced taxa. [Moreover, indicating] that a survey of contemporary samples only (as undertaken for the majority of invasive species studies) would be insufficient to identify potential source populations and occurrence of multiple introductions.

But, we can do more than tracing invasions?
Hornett et al. (2009) revealed a profound shift in several populations studied using museum and contemporary samples of butterflies and male-killing Wolbachia bacteria:

  • two populations were female-biased due to spread of bacteria
  • one population evolved from female-biased back to parity because infections lost male-killing activity
  • one population fluctuated widely in sex ratio due to varying frequency of male killing bacteria

Vandepitte et al. (2014) recently published one of the first studies using SNPs on herbarium material. They found strong divergence in flowering time genes during the establishment of the Pyrenean rocket. Rapid genetic adaptation preceded the spread of this species. The use of old non-native herbarium specimens provided knowledge regarding historical genetic structure and makeup of introduced populations.
As the tools at our disposal continue to increase, it seems an appropriate time to make use of these fantastic repositories of genetic material.

Herbarium seaweed specimens at the Natural History Museum London © S.A. Krueger-Hadfield

Herbarium specimens at the Natural History Museum London © S.A. Krueger-Hadfield


References
Dormontt EC et al. (2014) Genetic Bottlenecks in Time and Space: Reconstructing Invasions from Contemporary and Historical Collections. PLoS ONE 9: e106874
Hornett EA et al. (2009) Rapidly shifting sex ratio across a species range. Curr. Biol. 19, 1628-1631
Lavoie C (2013) Biological collections in an ever changing world: Herbaria as tools for biogeographical and environmental studies. Perspect. Plant Ecol. Evol. Syst. 15, 68-76
Martin MD et al. (2014) Herbarium specimens reveal a historical shift in phylogeographic structure of common ragweed during native range disturbance. Mol. Ecol. 23, 1701-1716
Provan J et al. (2007) Tracking biological invasions in space and time: elucidating the invasive history of the green alga Codium fragile using old DNA. Diversity Distrib. 14, 343-354
Reem E, et al. (2013) Long term population genetic structure of an invasive urochordate: the ascidian Botryllus schlosseri. Biol. Invasions 15, 225-241
Shapiro B, et al. (2002) Flight of the dodo. Science 295, 1683
Silvertown J, et al. (2006) The Park Grass Experiment 1856-2006: its contribution to ecology. J. Ecol. 94, 801-814
Vandepitte K et al. (2014) Rapid genetic adaptation precedes the spread of an exotic plant species. Mol. Ecol. 23, 2157-2164
Wandeler P, et al. (2007) Back to the future: museum specimens in population genetics. TREE 22, 634-642

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