A mechanism of extreme growth and reliable signaling in sexually selected ornaments and weapons

Science

Volumn 337, Issue 6096, 2012, Pages 860-864

  Emlen, Douglas J ^a   Warren, Ian A ^b   Johns, Annika ^a   Dworkin, Ian ^c   Lavine, Laura Corley ^b  

^a UNIVERSITY OF MONTANA   (United States)

^b WASHINGTON STATE UNIVERSITY   (United States)

^c MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN; SOMATOMEDIN;

ANIMAL; CYTOLOGY; ENZYME; HORN; NUTRITIONAL REQUIREMENT; PHYSIOLOGICAL RESPONSE; SEXUAL SELECTION; SIGNAL;

ARTICLE; BEETLE; BIOLOGICAL TRAIT; BIRD; CRAB; EUPLECTES PROGNE; GROWTH; HORN; NONHUMAN; NUTRITION; ORNAMENTAL SPECIES; PRIORITY JOURNAL; PROTEIN EXPRESSION; RED DEER; REGULATORY MECHANISM; RHINOCEROS BEETLE; SEXUAL SELECTION; SIGNAL TRANSDUCTION; TRYPOXYLUS DICHOTOMUS; UCA TETRAGONON; WEAPON;

ANIMALIA; ORYCTES RHINOCEROS;

EID: 84865085712     PISSN: 00368075     EISSN: 10959203     Source Type: Journal    
DOI: 10.1126/science.1224286     Document Type: Article

References (37)

1. C. Darwin, The Descent of Man and Selection in Relation to Sex (Random House, Modern Library, New York, 1871).
2. J. W. Bradbury, S. L. Vehrencamp, Principles of Animal Communication (Sinauer, Sunderland, MA, 2011).
3. J. Maynard Smith, D. Harper, Animal Signals (Oxford Univ. Press, Oxford, 2004).
4. W. A. Searcy, S. Nowicki, The Evolution of Animal Communication: Reliability and Deception in Signaling Systems (Princeton Univ. Press, Princeton, NJ, 2005).
5. S. Cotton, K. Fowler, A. Pomiankowski, Evolution 58, 1038 (2004).
6. R. Bonduriansky, L. Rowe, Evolution 59, 138 (2005).
7. R. J. Knell, N. Fruhauf, K. A. Norris, Ecol. Ent. 24, 323 (1999).
8. R. V. Alatalo, J. Höglund, A. Lundberg, Biol. J. Linn. Soc. Lond. 34, 363 (1988).
9. S. Fitzpatrick, Biol. J. Linn. Soc. Lond. 62, 145 (1997).
10. J. J. Cuervo, A. P. Møller, J. Evol. Biol. 22, 1503 (2009).
11. R. A. Johnstone, Biol. Rev. Camb. Philos. Soc. 70, 1 (1995).
12. L. Rowe, D. Houle, Proc. Biol. Sci. 263, 1415 (1996).
13. Y. Iwasa, A. Pomiankowski, J. Theor. Biol. 200, 97 (1999).
14. S. Cotton, K. Fowler, A. Pomiankowski, Proc. Biol. Sci. 271, 771 (2004).
15. R. Bonduriansky, Am. Nat. 169, 9 (2007).
16. A more complete description of this pathway and references are provided in the supplementary materials.
17. For this study, we define tissue sensitivity as the extent to which variations in the level of hormone signal influence the rate of cell proliferation via activity of the insulin/IGF pathway. Insensitive tissues grow to roughly the same final size regardless of circulating insulin/IGF concentrations, whereas the amounts of growth of sensitive tissues are strongly regulated by signal levels. Tissue sensitivity is often equated with receptor density. However, in this case, altered expression of any number of downstream genes in the pathway could change the responsiveness of a tissue to insulin/IGF signals. Indeed, in the best-studied example to date, reduced insulin sensitivity in a specific tissue (genitalia) in Drosophila, resulted from lowered levels of expression of a "downstream" element of the insulin-signaling pathway, FOXO, and not from tissue differences in expression of the insulin receptor (21).
18. A. W. Shingleton, W. A. Frankino, T. Flatt, H. F. Nijhout, D. J. Emlen, Bioessays 29, 536 (2007).
19. A. W. Shingleton, C. K. Mirth, P. W. Bates, Proc. Biol. Sci. 275, 1875 (2008).
20. A. W. Shingleton, J. Das, L. Vinicius, D. L. Stern, PLoS Biol. 3, e289 (2005).
21. H. Y. Tang, M. S. B. Smith-Caldas, M. V. Driscoll, S. Salhadar, A. W. Shingleton, PLoS Genet. 7, e1002373 (2011).
22. Results, as well as all methods for this paper, are in the supplementary materials.
23. A description of these studies is in the supplementary materials.
24. A. Zahavi, J. Theor. Biol. 53, 205 (1975).
25. A. Grafen, J. Theor. Biol. 144, 517 (1990).
26. M. Andersson, Evolution 40, 804 (1986).
27. P. D. Lorch, S. Proulx, L. Rowe, T. Day, Evol. Ecol. Res. 5, 867 (2003).
28. J. L. Tomkins, J. Radwan, J. S. Kotiaho, T. Tregenza, Trends Ecol. Evol. 19, 323 (2004).
29. G. A. Parker, J. Theor. Biol. 47, 223 (1974).
30. M. Enquist, O. Leimar, J. Theor. Biol. 102, 387 (1983).
31. A. Pomiankowski, Proc. R. Soc. Lond. B Biol. Sci. 231, 123 (1987).
32. R. Bonduriansky, T. Day, Evolution 57, 2450 (2003).
33. A. Kodric-Brown, R. M. Sibly, J. H. Brown, Proc. Natl. Acad. Sci. U.S.A. 103, 8733 (2006).
34. J. S. Kotiaho, Biol. Rev. Camb. Philos. Soc. 76, 365 (2001).
35. J. F. Husak, J. G. Swallow, Behaviour 148, 1 (2011).
36. In principle, selection on poor-quality males to cheat could lead to evolutionary modifications to the underlying developmental mechanism that buffered expression of the exaggerated trait from the influence of male condition (i.e., that decreased sensitivity to insulin/IGF signals). In this event, the condition sensitivity of trait expression and among-male variability in trait size would decrease (as in male genitalia of these beetles), reducing the reliability of the size of the trait as a signal of male quality. We are aware of no instances in which exaggerated sexually selected signal traits presently display condition insensitivity and/or reduced among-individual variation. This could be because once the traits become exaggerated, their costs reinforce signal honesty and select against cheating males. Or it could reflect the fact that once subsequent insensitivity to insulin/IGF evolves in an exaggerated trait, its reliability as a signal diminishes, favoring receivers who ignore the trait and focus instead on other signals.
37. C. E. Oufiero, T. Garland Jr., Funct. Ecol. 21, 676 (2007).