Nature 380, 155 - 156 (14 March 1996); doi:10.1038/380155a0

Non-mutualistic yucca moths and their evolutionary consequences

Olle Pellmyr, James Leebens-Mack & Chad J. Huth

Department of Biology, Vanderbilt University, Nashville, Tennessee 37235, USA

INTERSPECIFIC mutualisms are regarded as having evolved from antagonistic or commensalistic interactions, with most mutualisms remaining facultative but some having coevolved into obligate reciprocal dependency¹⁻⁴. Underlying mutualism is an intrinsic conflict between the parties, in that each is under selection for increased exploitation of the other³⁻⁷. Theoretical models suggest that this conflict is a source of evolutionary instability, and that evolution of 'cheating' by one party may lead to reciprocal extinction^4,6,7. Here we present phylogenetic evidence for reversal of an obligate mutualism: within the yucca moth complex, distinct cheater species derived from obligate pollinators inflict a heavy cost on their yucca hosts by laying their eggs but not pollinating the yucca. Phylogenetic data show the cheaters to have existed for a long time. Coexisting pollinators and cheaters are not sister taxa, supporting predictions that evolution of cheating within a single pollinator is evolutionary unstable. Several lines of evidence support a hypothesis that host shifts preceded the reversal of obligate mutualism. Host or partner shifts is a mechanism that can provide a route of evolutionary escape among obligate mutualists in general.

References

1.	Thompson, J. N. The Revolutionary Process (University of Chicago Press, 1994).
2.	Gargas, A., dePriest, P. T., Grube, M. & Tehler, A. Science 268, 1492−1495 (1995). | PubMed | ISI | ChemPort |
3.	Axelrod, R. & Hamilton, W. D. Science 242, 1385−1390 (1981).
4.	Bull, J. J. & Rice, W. R. J. theor. Biol. 149, 63−74 (1991). | PubMed | ISI | ChemPort |
5.	Pellmyr, O. & Huth, C. J. Nature 372, 257−260 (1994). | Article | ISI | ChemPort |
6.	Trivers, R. L. Q. Rev. Biol. 46, 35−57 (1971). | Article | ISI |
7.	Soberon Mainero, J. & Martinez del Rio, C. in The Biology of Mutualism (ed. Boucher, D. H.) 192−216 (Oxford Univ. Press, New York, 1985).
8.	Riley, C. V. Am. Mo. bot. Gdn 3, 99−158 (1892).
9.	Powell, J. A. Trends Ecol. Evol. 7, 10−14 (1992). | Article |
10.	Richter, K. S. & Weis, A. E. Nature 376, 557−558 (1995). | Article | PubMed | ChemPort |
11.	Keeley, J. E., Keeley, S. C. & Ikeda, D. A. Am. Midl. Nat. 115, 1−9 (1986).
12.	Pellmyr, O. & Thompson, J. N. Proc. natn. Acad. Sci. U.S.A. 89, 2927−2929 (1992). | ChemPort |
13.	Davis, D. R. U.S. natn. Mus. Bull. 255, 1−170 (1967).
14.	Miles, N. J. J. Lepid. Soc. 37, 207−216 (1983).
15.	Tyre, A. J. & Addicott, J. F. Oecologia 94, 173−175 (1993). | Article |
16.	Riley, C. V. Proc. Am. Ass. Advmt Sci. 29, 617−639 (1881).
17.	Feist, M. A. thesis, Univ. Cincinnati (1995).
18.	Felsenstein, J. Phylogenetic Inference Package (PHYLIP) version 3.5c (University of Washington, 1993).
19.	Kimura, M. J. molec. Evol. 16, 111−120 (1980). | PubMed | ISI | ChemPort |
20.	Wright, S. The Theory of Gene Frequencies Vol. 2 (Univ. of Chicago Press, 1969).
21.	Dawkins, R. The Selfish Gene, 2nd edn (Oxford Univ. Press, 1989).
22.	Vickery, W. L., Giraldeau, L.-C., Templeton, J. J., Kramer, D. L. & Chapman, C. A. Am. Nat. 137, 847−863 (1991). | Article |
23.	Yamauchi, A. Am. Nat. 145, 434−456 (1995). | Article |
24.	Galil, J. & Eisikowitch, D. Tijdschr. Ent. 112, 1−13 (1969).
25.	Wiebes, J. T. Proc. K. ned. Akad. Wet. 97, 491−495 (1994).
26.	Kishino, H. & Hasegawa, M. J. molec. Evol. 29, 170−179 (1989). | PubMed | ChemPort |
27.	Brown, J. L., Pellmyr, O., Thompson, J. N. & Harrison, R. G. Ann. ent. Soc. Am. 87, 795−802.
28.	McKelvey, S. D. Yuccas of the Southwestern United States (Arnold Arboretum, Jamaica Plain, MA, 1938, 1947).
29.	Swofford, D. L. Phylogenetic Analysis Using Parsimony, version 3.1 (Illinois Natural History Survey, Champaign, Urbana, IL, 1993).
30.	Clary, D. O. & Wolstenholme, D. R. J. molec. Evol. 22, 252−571 (1985). | PubMed | ISI | ChemPort |