Review
Back to the future: museum specimens in population genetics

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Museums and other natural history collections (NHC) worldwide house millions of specimens. With the advent of molecular genetic approaches these collections have become the source of many fascinating population studies in conservation genetics that contrast historical with present-day genetic diversity. Recent developments in molecular genetics and genomics and the associated statistical tools have opened up the further possibility of studying evolutionary change directly. As we discuss here, we believe that NHC specimens provide a largely underutilized resource for such investigations. However, because DNA extracted from NHC samples is degraded, analyses of such samples are technically demanding and many potential pitfalls exist. Thus, we propose a set of guidelines that outline the steps necessary to begin genetic investigations using specimens from NHC.

Introduction

Given that evolution is change over time, documenting and understanding temporal patterns has long been at the heart of evolutionary studies. In disciplines such as palaeontology, inferences about evolutionary processes are drawn from the analyses of temporal patterns in the fossil record. Similarly, our understanding of microevolutionary processes (i.e. changes in gene frequencies over time) has often involved the analyses of records taken over several years; Dobzhanksy's [1] early studies of microevolution among Drosophila used this approach, a tradition that continues among students of this model organism today [2]. However, such microevolutionary studies were often limited to certain taxa and questions because the time available to document temporal changes was often limited to a few generations.

How can these limitations be overcome? Long term studies, running over several decades, are one possibility and they are yielding fascinating insights, for example, into the role of reinforcement and character displacement in adaptive radiation and speciation 3, 4. Another approach, which gives longer time series, is to extend the data back in time using well preserved fossil samples or specimens from natural history collections (NHC). Here, we review the use of specimens from NHC for the study of evolutionary change. We aim to increase awareness of both the methodological limitations involved in using molecular methods with NHC specimens and their future potential.

We focus on studies of evolutionary change rather than the widespread use of NHC specimens in phylogenetics and phylogeography (e.g. Ref [5]) or pathogen origin and dynamics (e.g. Ref [6]). Similarly, we limit ourselves to studies of NHC specimens and do not consider studies of ancient DNA (Box 1; see 7, 8 for excellent reviews on the latter). Although ancient DNA studies have yielded spectacular results 9, 10, they will remain restricted to a relatively small set of species because the samples required for such work are rare and difficult to obtain. By contrast, NHC specimens generally cover a broader taxonomic range and are more easily obtained, thus enabling a wider range of questions and taxa to be studied.

Section snippets

NHC samples in conservation genetics

A large proportion of empirical studies of NHC samples published to date contrast past and recent genetic diversity in threatened and endangered populations or species (Table 1). Many now endangered or extinct populations and species became so within the past two centuries [11], a time period that coincides with the establishment of the majority of NHC (but see Ref [12]). As a result, specimens stored in NHC often represent the genetic diversity of populations shortly before significant

NHC samples in evolutionary biology

Fisher and Ford [37] provided an early example of the use of NHC specimens to study evolutionary change directly. Their 1947 study of the spread of the medionigra gene among the scarlet tiger moth (Callimorpha dominula) provided clear evidence for gene frequency change owing to natural selection. Since then, surprisingly few studies have taken advantage of the evolutionary history preserved in NHC samples to investigate the molecular footprint of selection. One such study investigated the

Pitfalls and precautions

NHC hold an unchallenged wealth of specimens that reflect past and current biodiversity of our planet. However, molecular studies based on historical samples are challenging because genotype and sequence data obtained by PCR are often error prone. Consequently, precautions are needed to guarantee reliable genetic data.

Prospects

In the near future, advances in molecular technologies will enable access to more and more genetic information from specimens archived in NHC. This progress will allow us to shift from neutral genetic markers to specific genes under selection.

Conclusions

Analyses of DNA from NHC samples have played an important role in conservation genetics by identifying processes that have shaped current levels of genetic diversity. A strong taxonomic bias is apparent among the studies to date (Table 1). Vertebrates and particularly fish predominate, whereas studies on plants and invertebrates are surprisingly rare. This bias might, in part, have arisen from biases in sample availability, conservation interests and methodological constraints, but the lack of

Acknowledgements

We thank Mark Beaumont, Love Dalén, Felix Gugerli, Michael Hofreiter and Phil Morin for helpful discussions and comments. Homayoun Bagheri, Jim Groombridge, Ken Petren and three anonymous referees made helpful comments on an earlier version of this article.

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