Culture and Genetic Evolution in Whales H. Whitehead (1) explains low nucleotide diversities in the control region of the mito- chondrial DNA (mtDNA) of matrilineal whale species with the use of a theory developed for molecular “hitchhiking,” in which diversity at a neutral locus is reduced by selection at a linked locus. As appealing as this idea is, we question the strength of the evidence presented to support a connection between whale culture and genetic variation. In the proposed model [figure 1 in (1)], if nonmatrilineal transmission is greater than 0.5%, then mtDNA diversity is little reduced [figure 1D in (1)]. We agree that killer whales, pilot whales, and sperm whales show the best evidence for matrilineal social struc- ture (2), yet even in these species the param- eters of the model are likely not met. This is especially so in the case of sperm whales, where recent studies show that sperm whale units (3) and groups (4 ) are composed of both related and unrelated individuals, at numbers significantly above the 0.5% threshold (1) at which mtDNA diversity is little reduced. If unrelated individuals co-occur within a group, then the cultural transmission of ad- vantageous information must be done in such a way that members outside a particular ma- triline are not privy to it. The model is presented to demonstrate the feasibility of a cultural trait that devastates mtDNA diversity. After such a trait sweeps through the population, molecular diversity should regenerate. Even if continual cultural innovation suppresses regeneration of diver- sity within geographic populations, one would not expect divergence among isolated popu- lations to remain low. A good example of this problem would be short-finned pilot whales, whose distribution is generally thought to be restricted to warm waters. It is difficult to imagine selective sweeps, cultural or other- wise, acting to maintain low inter-ocean diversity. To us, the finding of low inter- ocean mtDNA diversity suggests continuing selection. The data summarized to support the re- port’s hypothesis [table 1 in (1)] deserve close scrutiny. In comparative studies, it is necessary that the playing field be level. Sam- ples need to be collected over comparable scales (geographic, temporal, and numerical), which is no trivial task in ocean-dwelling species. Moreover, the unsettled nature of cetacean alpha level taxonomy affects our ability to accurately compare estimates of molecular diversity across taxa. For example the “killer whale” and the “bottlenose dol- phin” are names given to what we now un- derstand to be complexes comprised of ge- netically distinct inshore and offshore taxa and suggested to be separate species (5 ). Table 1 in the report may be presenting di- versity levels calculated both within species and within genera. There is strikingly low control region di- versity in some cetacean species, all the more remarkable given the vast geographic ranges of these animals. With the above con- cerns in mind, we advocate the investigation of a more general question: What factors could reduce mtDNA diversity in whales, and how does their marine existence affect this pattern? Sarah L. Mesnick Barbara L. Taylor Richard G. Le Duc Sergio Escorza Trevin ˜o Greg M. O’Corry-Crowe Andrew E. Dizon Southwest Fisheries Science Center, National Marine Fisheries Service, National Oceanographic and Atmospheric Administration, La Jolla, CA 92038, USA E-mail: sarahlyn@caliban.ucsd.edu References 1. H. Whitehead, Science 282, 1708 (1998). 2. R. C. Connor et al., Trends Ecol. Evol. 13, 228 (1998). 3. J. Christal, thesis, Dalhousie University, Halifax (1998). 4. K. Richard et al., Proc. Natl. Acad. Sci. U.S.A. 93, 8792 (1996); J. Bond, thesis, Cambridge University (1999); S. Mesnick et al., in preparation. 5. B. Curry, thesis, Texas A & M University, Galveston, TX (1997); A. R. Hoelzel, M. Dahlheim, S. J. Stern, J. Hered. 89, 121 (1998); R. Hoelzel, C. W. Potter, P. B. Best, Proc. R. Soc. London B. 265. 1177 (1998). 12 February 1999; accepted 10 May 1999 Whitehead (1) found low mtDNA diversity in whales with a matrilineal social structure. He interpreted this finding as resulting from “hitchhiking” of neutral mtDNA alleles through selection on maternally transmitted cultural traits. The matrilineal structure of Globicephal- as melas, the long finned pilot whale, has been studied in great detail by the use of molecular markers (2). Thus, one might ask if the current knowledge about the social struc- ture in this species is compatible with the predictions and requirements for transmitted cultural traits. Are cultural traits transmitted through females only? Both sexes are ob- served in the social groups, and thus an ad- vantageous behavior may be rapidly adapted from males. With the use of polymorphic microsatellite loci, Amos et al. (2) demon- strated that males in a social group (pod) are related to the females, but do not reproduce in their natal group. It is generally assumed that, during the mating period, males tempo- rarily leave their group, mate with females from a different group, and return to their natal group. Thus, in pilot whales, cultural transmission need not be limited to females and could still result in a reduced mtDNA variability. While the behavior of pilot whales is fully consistent with the proposed cultural trans- mission, more scrunity should be applied to the molecular data on which the hypothesis is based. Whitehead calculated Tajima’s “D” statistic (3) to exclude the possibility that the reduced mitochondrial variability is the result of an advantageous base substitution in the mtDNA that is sweeping through the popula- tion. The absence of a significant value of D was taken as evidence against a putative non- neutral behavior of mtDNA causing the ob- served low mtDNA variability. Although this conclusion may be correct, the alternative scenario of maternally transmitted cultural traits does not differ qualitatively. In both cases, it is assumed that the target of selec- tion resides outside the sequenced part of the mtDNA. Thus, hitchhiking of the se- quenced DNA region together with the tar- get of selection is assumed. The effect on the sequenced mtDNA region is expected to be the same, whether or not a base substitution in the mtDNA or cultural trans- mission through the bearer of the mtDNA is causing the selective advantage. Conse- quently, the predictions for Tajima’s D are identical in both cases. A nonsignificant value of D could also be regarded as a rejection of the cultural transmission hy- pothesis of Whitehead. In summary, the data presented by White- head do not provide evidence for or against the hypothesis of maternally transmitted cul- tural traits that confer selective advantage. Low mtDNA diversity could be a result of the effective population size of these species sim- ply being smaller than that of the other spe- cies surveyed. Census population sizes are known to be an inaccurate estimator of effec- tive population sizes (4 ), thus, data from nuclear sequences are needed for an indepen- dent estimate of the effective population size. Microsatellites, for which some data have been already collected (2, 5, 6 ), may not be the most appropriate genetic marker to test this hypothesis, given the well-documented problem of ascertainment bias (7 ) as well as large differences between individual micro- satellite loci (8). Christian Schlo ¨tterer Institut fu ¨r Tierzucht und Genetik, Josef-Baumann Gasse 1, A-1210 Wien, Austria E-mail: christian.schloetterer@vu-wien.ac.at T ECHNICAL C OMMENT www.sciencemag.org SCIENCE VOL 284 25 JUNE 1999 2055a on March 8, 2016 Downloaded from on March 8, 2016 Downloaded from on March 8, 2016 Downloaded from on March 8, 2016 Downloaded from on March 8, 2016 Downloaded from