Trends in Ecology & Evolution
ReviewBack to the future: museum specimens in population genetics
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.
References (85)
New developments in museum-based informatics and applications in biodiversity analysis
Trends Ecol. Evol.
(2004)Noninvasive genetic sampling: look before you leap
Trends Ecol. Evol.
(1999)A high frequency of sequence alterations is due to formalin fixation of archival specimens
Am. J. Pathol.
(1999)Assessing ancient DNA studies
Trends Ecol. Evol.
(2005)SNPs in ecology, evolution and conservation
Trends Ecol. Evol.
(2004)Towards the analysis of the genomes of single cells: further characterisation of the multiple displacement amplification
Gene
(2006)Genetic monitoring as a promising tool for conservation and management
Trends Ecol. Evol.
(2007)Landscape genetics: combining landscape ecology and population genetics
Trends Ecol. Evol.
(2003)Genetics of natural populations IX. Temporal changes in the composition of populations of Drosophila pseudoobscura
Genetics
(1943)Global genetic change tracks global climate warming in Drosophila subobscura
Science
(2006)
The Park Grass Experiment 1856-2006: Its contribution to ecology
J. Ecol.
Evolution of character displacement in Darwin's finches
Science
Flight of the dodo
Science
Wheat archive links long-term fungal pathogen population dynamics to air pollution
Proc. Natl. Acad. Sci. U. S. A.
Genetic analyses from ancient DNA
Annu. Rev. Genet.
Ancient DNA
Nat. Rev. Genet.
Genetic response to climatic change: insights from ancient DNA and phylochronology
PLoS Biol.
Microevolution and mega-icebergs in the Antarctic
Proc. Natl. Acad. Sci. U. S. A.
Mammal population losses and the extinction crisis
Science
Prehistoric decline of genetic diversity in the nene
Science
The use of museum specimens to reconstruct the genetic-variability and relationships of extinct populations
Experientia
The ghost of genetic diversity past: historical DNA analysis of the greater prairie chicken
Am. Nat.
Genetic consequences of a demographic bottleneck in the Scandinavian arctic fox
Oikos
Loss of microsatellite diversity and low effective population size in an overexploited population of New Zealand snapper (Pagrus auratus)
Proc. Natl. Acad. Sci. U. S. A.
‘Ghost’ alleles of the Mauritius kestrel
Nature
Temporal changes in allele frequencies and low effective population size in greater prairie-chickens
Mol. Ecol.
Impact of a population bottleneck on symmetry and genetic diversity in the northern elephant seal
J. Evol. Biol.
Loss of genetic diversity in the endemic Hector's dolphin due to fisheries-related mortality
Proc. R. Soc. Lond. B Biol. Sci.
Population structure and loss of genetic diversity in the endangered white-headed duck, Oxyura leucocephala
Conserv. Genet.
Genetic evidence for the persistence of the critically endangered Sierra Nevada red fox in California
Conserv. Genet.
Legacy lost: genetic variability and population size of extirpated US grey wolves (Canis lupus)
Mol. Ecol.
Stability in the historical pattern of genetic structure of Newfoundland cod (Gadus morhua) despite the catastrophic decline in population size from 1964 to 1994
Conserv. Genet.
Appraisal of the consequences of the DDT-induced bottleneck on the level and geographic distribution of neutral genetic variation in Canadian peregrine falcons, Falco peregrinus
Mol. Ecol.
Genetic consequences of population decline in the European otter (Lutra lutra): an assessment of microsatellite DNA variation in Danish otters from 1883 to 1993
Proc. R. Soc. Lond. B Biol. Sci.
Estimation of effective population sizes from data on genetic markers
Philos. Trans. R. Soc. Lond. B Biol. Sci.
Long-term effective population sizes, temporal stability of genetic composition and potential for local adaptation in anadromous brown trout (Salmo trutta) populations
Mol. Ecol.
Historical analysis of genetic variation reveals low effective population size in a northern pike (Esox lucius) population
Genetics
Temporal change in genetic structure and effective population size in steelhead trout (Oncorhynchus mykiss)
Mol. Ecol.
The history of effective population size and genetic diversity in the Yellowstone grizzly (Ursus arctos): Implications for conservation
Proc. Natl. Acad. Sci. U. S. A.
Effective population sizes and temporal stability of genetic structure in Rana pipiens, the northern leopard frog
Evolution Int. J. Org. Evolution
Population fragmentation leads to spatial and temporal genetic structure in the endangered Spanish imperial eagle
Mol. Ecol.
Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America
Proc. Natl. Acad. Sci. U. S. A.
Cited by (478)
A Life in Fragments: The Ecology, Behavior, and Conservation of the Recently Described Parecis Plateau Titi Monkey (Plecturocebus parecis)
2024, International Journal of PrimatologyUnlocking the genomes of formalin-fixed freshwater fish specimens: An assessment of factors influencing DNA extraction quantity and quality
2023, North American Journal of Fisheries Management