Mate Choice and Evolutionary Genetics in Xiphophorus hybrid zones

The evolution of complex, multivariate courtship displays continues to present a puzzle in the field of sexual selection. How do psychological mechanisms of female mate choice interact with multivariate signal complexes in males to drive the evolution of male traits and female preferences? We are using replicated natural hybrid zones of the swordtail fish Xiphophorus malinche and X. birchmanni, which enable us to characterize male signal complexes and multivariate female mating preferences, identify genetic loci underlying these traits and preferences, and study how these loci evolve in natural populations. We are currently focusing on three basic questions about the evolution of multivariate traits and preferences.

1. How does multivariate trait space align with multivariate preference space, and how does hybridization influence this alignment? A number of recent studies have shown that female mating preferences for multiple traits can be incongruent with variation in male traits; for examples, females may show opposing preferences for two traits that are positively correlated in males. Natural hybridization may act to break correlations among traits and among preferences. The alignment of female preferences onto male traits has a fundamental impact on the strength of sexual selection and on the direction of trait and preference evolution. To compare male trait and female preference spaces, we sample variation in multiple visual traits in males from hybrid and parental populations. We use these data to construct an array of computer-animated stimuli, which we present to females using a high-throughput, automated tracking system that permits intense sampling of multivariate preference space in large numbers of individuals.

2. How does trait-preference alignment influence population structure? How do female preferences impact mating outcomes in the wild? If multivariate male traits and multivariate female preferences are completely misaligned, mating should be random with respect to these traits; while if traits and preferences are aligned, populations should show assortative mating with respect to traits and preferences. We are sequencing transcriptomes of male and female X. birchmanni and X. malinche, and using these to generate a single-nucleotide-polymorphism marker array. We will then use admixture mapping to identify chromosomal regions associated with male traits and female preferences. We will use genotypic data on wild-caught females and their offspring to infer paternal genotypes. This will allow us to evaluate whether individual, behavioral measures of multivariate mating preference are predictive of realized mating outcomes in the wild.

3. How do the genetics of female preference drive trait evolution? Natural hybrids between species with divergent mating biases are uniquely suited to identifying genomic regions associated with differences in female preference. Sexual communication in Xiphophorus hybrid zones is rapidly evolving, with dramatic phenotypic shifts across multiple hybrid zones over periods of only a few years. We will be able to track how chromosomal regions associated with specific traits and preferences are moving through hybrid zones over space and time, as well as evaluate how genetic associations among traits are evolving. Admixture mapping allows us to identify how genetic constraints on multiple traits and multiple preferences (such as pleiotropic effects of a single chromosomal region on preference for two distinct male traits) explain the alignment between traits and preferences.

We address these questions via (a) high-throughput, high-resolution behavioral mapping of female preference space, using state-of-the-art animation playback techniques in conjunction with automated behavioral tracking; (b) identification of chromosomal regions associated with traits and preferencesusing the recently developed technique of admixture mapping; and (c) measurement of trait-preference associations in the wild using markers associated with these chromosomal regions. 

 

Publications

  1. G.G. Rosenthal and M. J. Ryan, in press. Multiple visual cues, receiver psychology, and signal evolution in pygmy swordtails. In Viviparous Fishes II, Maricarmen Uribe Aranzabal ed.
  2. G.G. Rosenthal and F.J. García de León, in press. Speciation and hybridization. In Ecology and Evolution of Poeciliid Fishes (I. Schlupp, A. Pilastro, J. Evans eds.), University of Chicago Press.
  3. H.S. Fisher and G.G. Rosenthal, 2010. Relative abundance of Xiphophorus fishes and its effect on sexual communication. Ethology [PDF]
  4. S.W. Coleman, Z.W. Culumber, A. Meaders, J. Henson and G.G. Rosenthal, 2009. Inducible molecular defenses, ultraviolet radiation, and melanomagenesis in natural Xiphophorus hybrids - a field-based investigation of lab-based cancer models. Env. Biol. Fish. [PDF]
  5. H.S. Fisher, S. Mascuch and G.G. Rosenthal, 2009. Multivariate male traits misalign with multivariate female preferences in the swordtail fish, Xiphophorus birchmanni. Anim. Behav. [PDF]
  6. K. Summers, K. Roney, J. da Silva, G. Capraro, B.J. Cuthberson, S. Kazianis, G.G. Rosenthal, M.J. Ryan and T.J. McConnell, 2009. Divergent patterns of selection on the DAB and DXB MHC Class II loci in Xiphophorus fishes. Genetica 135: 379-390. [PDF]
  7. J. Buckingham, B.B.M. Wong and G.G. Rosenthal, 2007. Shoaling decisions in female swordtails: how do fish gauge group size? Behaviour 144: 1333-1346. [PDF]
  8. H.S. Fisher and G.G. Rosenthal, 2007. Male swordtails court with an audience in mind. Biol. Lett. 3: 5-7. [PDF]
  9. S.W. Coleman and G.G. Rosenthal, 2006. Swordtail fry attend to chemical and visual cues in detecting predators and conspecifics. PLoS One 1: e118. [PDF]
  10. H.S. Fisher and G.G. Rosenthal, 2006b. Hungry females show stronger mating preferences. Behav. Ecol. 17: 979-981. [PDF]
  11. H.S. Fisher and G.G. Rosenthal, 2006a. Female swordtail fish use chemical cues to select well-fed mates. Anim. Behav. 72: 721-725. [PDF]
  12. G.G. Rosenthal and F. J. García de León, 2006. Sexual behavior, genes, and evolution in Xiphophorus. Zebrafish 3: 85-90. [PDF]
  13. H.S. Fisher, B.B.M. Wong and G.G. Rosenthal, 2006. Alteration of the chemical environment disrupts communication in a freshwater fish. Proceedings: Biological Sciences 273: 1187-1193. [PDF]
  14. B.B.M. Wong and G.G. Rosenthal, 2006. Female disdain for swords in a swordtail fish. Am. Nat. 167:136-140. [PDF]
  15. B.B.M. Wong, H.S. Fisher and G.G. Rosenthal, 2005. Species recognition by male swordtails via chemical cues. Behav. Ecol. 16:818-822. [PDF]
  16. B.B.M. Wong and G.G. Rosenthal, 2005. Shoal choice in swordtails when preferences conflict. Ethology 111: 179-186. [PDF]
  17. G.G. Rosenthal, X.F. de la Rosa Reyna, S. Kazianis, M.J. Stephens, D.C. Morizot, M.J. Ryan, and F.J. García de León, 2003. Dissolution of sexual signal complexes in a hybrid zone between the swordtails Xiphophorus birchmanni and Xiphophorus malinche (Poeciliidae). Copeia 2003: 299-307. [PDF]
  18. J. Kingston, G.G. Rosenthal and M.J. Ryan, 2003. The role of sexual selection in maintaining a colour polymorphism in the pygmy swordtail Xiphophorus pygmaeus. Anim. Behav. 65: 735-743. [PDF]
  19. G.G. Rosenthal, M.J. Ryan, and W.E. Wagner, Jr., 2002. Secondary loss of preference for swords in the pygmy swordtail Xiphophorus nigrensis (Pisces: Poeciliidae). Anim. Behav. 63: 37-45. [PDF]
  20. G.G. Rosenthal, T. Y. Flores Martinez, F. J. García de León, and M. J. Ryan, 2001. Shared preferences by predators and females for male ornaments in swordtails. Am. Nat. 158: 146-154. [PDF]
  21. M. J. Ryan and G.G. Rosenthal, 2001. Variation and selection in swordtails. In Model Systems in Behavioral Ecology, L. A. Dugatkin ed., Princeton University Press, 133-148. [PDF]
  22. G.G. Rosenthal and C. S. Evans , 1998. Female preference for swords in Xiphophorus helleri reflects a bias for large apparent size. Proc. Natl. Acad. Sci. 95: 4431-4436. [PDF]
  23. D. Clark, J. Macedonia, and G.G. Rosenthal, 1997. Testing video playback to lizards in the field. Copeia 1997: 421-423. [PDF]
  24. G.G. Rosenthal, C. S. Evans, and W. L. Miller, 1996. Female preference for a dynamic trait in the green swordtail, Xiphophorus helleri. Anim. Behav. 51: 811-820. [PDF]