Climate-Driven Range Expansion and Morphological Evolution in a Marine Gastropod
Abstract
Little is known about the phenotypic consequences of global climate change, despite the excellent Pleistocene fossil record of many taxa. We used morphological measurements from extant and Pleistocene populations of a marine gastropod (Acanthinucella spirata) in conjunction with mitochondrial DNA sequence variation from living populations to determine how populations responded phenotypically to Pleistocene climatic changes. Northern populations show little sequence variation as compared to southern populations, a pattern consistent with a recent northward range expansion. These recently recolonized northern populations also contain shell morphologies that are absent in extant southern populations and throughout the Pleistocene fossil record. Thus, contrary to traditional expectations that morphological evolution should occur largely within Pleistocene refugia, our data show that geographical range shifts in response to climatic change can lead to significant morphological evolution.
Get full access to this article
View all available purchase options and get full access to this article.
Already a Subscriber?Sign In
REFERENCES AND NOTES
1
Working Group FAUNMAP, Science 272, 1601 (1996).
2
Roy K., Valentine J. W., Jablonski D., Kidwell S. M., Trends Ecol. Evol. 11, 458 (1996).
3
Hewitt G. M., Biol. J. Linn. Soc. 58, 247 (1996).
4
Price T. D., Helbig A. J., Richman A. D., Evolution 51, 552 (1997).
5
Klicka J., Zink R. M., Science 277, 1666 (1997).
6
J. C. Avise, Phylogeography: The History and Formation of Species (Harvard Univ. Press, Cambridge, MA, 2000).
7
Valentine J. W., Paleobiology 15, 83 (1989).
8
Roy K., Jablonski D., Valentine J. W., Geology 23, 1071 (1995).
9
D. R. Lindberg, J. H. Lipps, in Evolutionary Paleobiology, D. Jablonski et al., Eds. (Univ. of Chicago Press, Chicago, IL, 1996), pp. 161–182.
10
Spight T. M., Nautilus 91, 67 (1977).
11
Gianniny G. L., Geary D. H., Veliger 35, 195 (1992).
12
Adult A. spirata were collected from high intertidal habitats between December 1999 and April 2000 by K.R. and/or D.P.B. at localities indicated in Fig. 1. A. paucilirata and A. punctulata were included as outgroups (20). Specimens were preserved in ≥70% ethanol and photographed for morphometric analyses, then crushed to extract tissue.
13
DNA was extracted from muscle tissue using cetyltrimethyl ammonium bromide (CTAB) methods, removing polysaccharide polymerase inhibitors with PhytoPure resin (Amersham). We amplified the DNA using primers HCOI (39) and LCOI+ (5'-GTCAACAAAATCATAAAGATATTGGAAC-3') and standard polymerase chain reaction profiles with an annealing temperature of 50°C. Products were directly sequenced in both directions on an ABI 377 sequencer, using the amplification primers. There were no indels and only three nonsynonymous substitutions within A. spirata (singletons in the Half Moon Bay, Leo Carillo, and Carlsbad populations). Parsimony networks were obtained with the software TCS 1.01 (D. Posada). Relationships among the three clades revealed by networks were polarized by means of neighbor-joining and parsimony methods (40), with A. paucilirata and A. punctulata (GenBank accession numbers and ) as outgroups. Various weighting schemes produced the same results. Analysis of molecular variation (19) and pairwise mismatch analyses (22) were performed with Arlequin 2.000 (41) based on simple pairwise distances.
14
Bernardi G., Evolution 54, 226 (2000).
15
Valentine J. W., Limnol. Oceanogr. 11, 198 (1966).
16
Roy K., Jablonski D., Valentine J. W., Proc. Natl. Acad. Sci. U.S.A. 95, 3699 (1998).
17
Burton R. S., Evolution 52, 734 (1998).
18
Gaylord B., Gaines S. D., Am. Nat. 155, 769 (2000).
19
Excoffier L., Smouse P. E., Quattro J. M., Genetics 131, 479 (1992).
20
Marko P. B., Vermeij G. J., Mol. Phylogenet. Evol. 13, 275 (1999).
21
M. E. Hellberg, K. Roy, data not shown.
22
Slatkin M., Hudson R. R., Genetics 129, 555 (1991).
23
Hellberg M. E., Evolution 48, 1829 (1994).
24
Marko P. B., Evolution 52, 757 (1998).
25
Zink R. M., Barrowclough G. F., Atwood J. L., Blackwell-Rago R. C., Conserv. Biol. 14, 1394 (2000).
26
G. L. Kennedy, thesis, University of California, Davis (1978).
27
Estimates are based on a nucleotide divergence rate of 2.4% per million years in COI in other gastropods [
Hellberg M. E., Vacquier V. D., Mol. Biol. Evol. 16, 839 (1999);
] and on coalescent analyses using FLUCTUATE (C. Cunningham, personal communication).
28
For living populations, morphological analyses were based on the same specimens as for sequence analysis; in a few localities, these were supplemented by additional specimens collected at the same time. Pleistocene specimens came from collections in the Natural History Museum of Los Angeles County and the California Academy of Sciences. The total number of Pleistocene specimens (179) used was similar to the total of living specimens (161) in order to minimize sample size effects. Ten positional landmarks on each photographed shell (Fig. 3) were used to obtain eight measurements with the image analysis software ImagePro Plus. All measurements were collected by one of us (D.P.B.) to maintain consistency. Morphological measurements were log-transformed, and a principal components analysis (PCA) using a correlation matrix was used to generate the shape morphospace (42). Only specimens >1.4 cm in total length were analyzed to control for ontogenetic changes in shell shape. Measurements were not size-standardized, and all data were combined into a single PCA. The first four principal components explained 95.8% of the total variance (PC1 = 80.1%, PC2 = 9.7%, PC3 = 3.9%, and PC4 = 2.1%). A second PCA using a covariance matrix produced similar results. A multivariate analysis of variance (MANOVA) of the principal component scores was used to test for spatial and temporal differences in morphology (Table 2). Further details about the measurements and PCA results are available from the authors.
29
Pease C. M., Lande R., Bull J. J., Ecology 70, 1657 (1989).
30
Case T. J., Taper M. L., Am. Nat. 155, 583 (2000).
31
Smith F. A., Betancourt J. L., Brown J. H., Science 270, 2012 (1995).
32
Hadly E. A., Kohn M. H., Leonard J. A., Wayne R. K., Proc. Natl. Acad. Sci. U.S.A. 95, 6893 (1998).
33
Chiba S., Paleobiology 24, 99 (1998).
34
Haffer J., Science 165, 131 (1969).
35
Losos J. B., Warhelt K. I., Schoener T. W., Nature 386, 70 (1997).
36
Huey R. B., Gilchrist G.W., Carlson M. L., Berrigan D., Serra L., Science 287, 308 (2000).
37
M. A. Bell, C. A. Andrews, in Evolutionary Ecology of Freshwater Animals, B. Streit, T. Städler, C. M. Lively, Eds. (Birkhäuser Verlag, Basel, Switzerland, 1997), pp. 323–363.
38
Rundle H. D., Nagel L., Boughman J. W., Schluter D., Science 287, 306 (2000).
39
Folmer O., Black M., Hoeh W., Lutz R., Vrijenhoek R., Mol. Mar. Biol. Biotechnol. 3, 294 (1994).
40
D. L. Swofford, PAUP*: Phylogenetic Analysis Using Parsimony (and Other Methods), version 4.062a (Sinauer, Sunderland, MA, 1998).
41
S. Schneider, D. Roessli, L. Excoffier, Arlequin: A Software for Population Genetics Data Analysis, version 2.000 (Genetics and Biometry Lab, Department of Anthropology, Univ. of Geneva, Switzerland, 2000).
42
Roy K., Foote M., Trends Ecol. Evol. 12, 277 (1997).
43
M. Nei, Molecular Evolutionary Genetics (Columbia Univ. Press, New York, 1987).
44
Tajima F., Genetics 105, 437 (1983).
45
We thank C. Cunningham, D. Jablonski, J. R. Kohn, R. Lande, P. Marko, J. Neigel, M. Noor, T. D. Price, M. Taylor, J. W. Valentine, J. Wares, and two anonymous reviewers for comments and/or discussions; P. Arbour-Reily and N. Crochet for technical help; and J. H. McLean, L. T. Groves (Natural History Museum of Los Angeles County), and P. D. Roopnarine (California Academy of Sciences) for access to museum collections and specimen loans. Supported by NSF grants (K.R. and M.E.H.).
Information & Authors
Information
Published In

Science
Volume 292 | Issue 5522
1 June 2001
1 June 2001
Submission history
Received: 22 February 2001
Accepted: 25 April 2001
Published in print: 1 June 2001
Authors
Metrics & Citations
Metrics
Article Usage
Altmetrics
Citations
Export citation
Select the format you want to export the citation of this publication.
Cited by
- Local Selection and Latitudinal Variation in a Marine Predator-Prey Interaction, Science, 300, 5622, (1135-1137), (2021)./doi/10.1126/science.1083437
- Climate Change, Human Impacts, and the Resilience of Coral Reefs, Science, 301, 5635, (929-933), (2021)./doi/10.1126/science.1085046
Loading...
View Options
Get Access
Log in to view the full text
AAAS login provides access to Science for AAAS Members, and access to other journals in the Science family to users who have purchased individual subscriptions.
- Become a AAAS Member
- Activate your AAAS ID
- Purchase Access to Other Journals in the Science Family
- Account Help
Log in via OpenAthens.
Log in via Shibboleth.
More options
Purchase digital access to this article
Download and print this article for your personal scholarly, research, and educational use.
Buy a single issue of Science for just $15 USD.
View options
PDF format
Download this article as a PDF file
Download PDF





