Summary of Some Studies of Túngara Frogs (July 2001)

Summary of Some Studies of Túngara Frogs (July 2001)

My primary research interest is in the mechanisms and evolution of animal communication. My approach has been to integrate Tinbergen’s “four questions”: function (adaptive significance), evolution (phylogenetic patterns), mechanisms, and acquisition of behavior (learning and development). Specifically, I have addressed how sexual selection and species recognition promote the evolution and phylogenetic patterns of signal diversity and the brain mechanisms that decode it.

My studies have been grounded in the behavior of animals in the wild and have utilized both experimental and observational approaches to the adaptive or functional significance of behavior. They have also expanded in two directions, one toward an understanding of neural mechanisms guiding behavior, and the other examining phylogenetic or macroevolutionary patterns of behavior. These studies, however, have done more than address questions at different levels of analysis. In addition, they have brought together diverse approaches to fundamental questions about complex social behavior, mostly sexual signaling, and demonstrated that a truly integrative approach as envisioned by Tinbergen is necessary for a deep and accurate understanding of how and why animals behave as they do (1, 2, 3). Such a diverse research program involves a number of collaborators. Almost all of this work is a collaboration with Dr. A.S. Rand of the Smithsonian Tropical Research Institute in Panama. Dr. Walt Wilczynski is responsible for the neurobiology, Dr. David Cannatella for the phylogenetics, an Dr. Steve Phelps for the artificial neural network studies.

I have been studying mechanisms and evolution of animal communication systems in frogs and fish. I will concentrate on studies of the túngara frog, Physalaemus pustulosus, as this has emerged as one of the premier systems for studying animal communication, in part because of the integrative nature of our studies.

Sexual Selection

Male frogs produce a species-specific advertisement call to attract females for mating (4,5,6). Key to understanding the túngara frog system is the fact that male túngara frogs facultatively alter call complexity. They produce a whine that can stand alone or be followed by one-six chucks. The whine is necessary and sufficient for attracting a female but males add chucks when vocal competing with other males (7). Although species recognition was known to be critical in the evolution of species-specific mate attraction signals in all animals, there had been scant attention paid to how sexual selection also might influence the evolution of such signals.

My earliest studies addressed the evolution of complex vocal signals in the túngara frog where I worked in Panama at the Smithsonian Tropical Research Institute (STRI). With a foundation from earlier, unpublished studies by A.S. Rand, I examined the significance of vocal variation, mate choice, and sexual selection. These studies showed how and why males increased call complexity, how this behavior was favored by sexual selection through female mate choice, and how female preference for lower frequency chucks biased matings in favor of large males (8, 9). This was one of the first (and perhaps the first) study to experimentally manipulate a male courtship trait to show that females attended to population variation in such signals (8). Later studies with M.D. Tuttle documented how frog-eating bats generate counter-selection on vocal advertisement—like female frogs, bats prefer more complex calls (10, 11, 12). Studies with G.W. Bartholomew showed that vocal advertising was an energetically very demanding activity, but that it cost no more to make calls with chucks than calls without chucks (13, 14, 15, 16). Much of the work on these topics was summarized in my book The Túngara Frog, A Study of Sexual Selection and Communication (Univ. Chicago Press, 1985).

Sexual Selection and Neuroethology

A next stage of studies involved long-term and ongoing collaboration with A.S. Rand, a resident scientist at STRI. We have continued to address the sexual communication system of túngara frogs but have supplemented our studies of behavioral ecology with those of neurobiology and phylogenetics (recent summaries include 17, 18).

Understanding the neural basis of signal recognition is an interesting pursuit in its own respect, the stuff of neuroethology. My interest in integrating neural mechanisms, however, is to understand the detailed biology of the preference and identify the locus of selection involved in the evolution of female preferences (19, 1, 4, 20, 21). When female preferences evolve something in the brain changes and we need to know what that is.

I have collaborated with W. Wilczynski to uncover the neural basis of signal decoding in túngara frogs, as well as cricket frogs (22, 23, 24, 25, 26). The túngara frog studies first characterized the spectral tuning of the túngara frog’s auditory system (27). In frogs, it is well know that there is a match between the emphasized frequencies in the mating call and the tuning of the frog’s two inner ear organs (reviewed in 5, 6). The neurophysiological results were combined with experimental tests of behavioral acoustic discrimination to begin to explain how the frogs decoded the complex mating call and why females preferred lower-frequency chucks of larger males (28, 29, 30, 26).

Sexual Selection, Neuroetholgy and Phylogenetics

Phylogeny has long played a role in studies of behavior but fell out of favor with the advent of sociobiology. But phylogenetics went through a revolution in North America when the writings of Hennig became available in English (31). The new techniques in this field proved to be powerful tools for critically testing patterns of behavioral evolution, as I showed in a early paper of phylogenetic patterns of frog calls that presaged a burst of activity in this area (32).

A phylogenetic dimension was added to the túngara frog studies with collaborations with D. Cannatella and D. Hillis. We used molecular data to reconstruct the phylogenetic relationships among the túngara frog and its close relatives (33). This information provided critical data to allow us to interpret patterns of signal receiver evolution which, in turn, led to our proposing the hypothesis of sensory exploitation (34, 27, 28). This posits that sexual selection may proceed by males evolving traits that exploit pre-existing sensory biases rather than signals and receivers coevolving. With an understanding of the neural mechanisms critical in preferring calls with chucks and lower frequency chucks, the phylogenetic information showed that males evolved chucks to exploit preexisting neural biases in túngara frogs. These neural mechanisms are found throughout closely related taxa even though only the túngara frog and its sister species produce complex calls (35). This hypothesis has been supported by a number of other taxa (reviewed in 20), and has become one of the more debated issues in the field in the last decade.

We further utilized this phylogenetic approach to construct ancestral calls and determine if female responses could be predicted by a phylogenetic component unrelated to overall signal similarity (36, 17, 37). We found that, indeed, evolution “leaves a footprint on the frog’s brain”, or more generally, that the signal decoding tasks performed by ancestors influence how these tasks are performed by current species. This latter hypothesis was critically borne out by computational neurobiology studies conducted with S.M. Phelps (38, 39). We showed that artificial neural networks predicted the response biases of real females, and that the predictability of the networks was better when these networks evolved through a series of calls that mimicked the calls of the túngara frogs direct ancestors rather than a random collection of calls. We have recently argued that our approach to the effect of historical contingency on brain function be applied more widely in the neural and cognitive sciences (21).

Our work continues to integrate behavioral ecology, neurobiology, and phylogenetics. Current studies are expanding the phylogenetic range of the study from the species group (six species) to the entire genus of about 30 species that ranges through much of the Amazon Basin and regions south. We are also focusing on microgeographic variation in the túngara frog using microsatellites to assess fine scale geographic variation in local signal preferences and testing the hypothesis that females assess call variation in inbreeding avoidance. Finally, we are concentrating on more cognitive issues such as how females are able to group call components from the same male in the cacophony of a chorus (auditory grouping), and the interaction between internal physiological state, experience, and female behavioral receptivity to auditory stimulation.

Although the research I have reviewed here concentrates on a single group of animals, these studies are providing text-book examples of how complex behavioral systems evolve in response to conflicting selection forces in the face of historical constraints.

References

1.  Ryan, M.J. 1990. Sensory systems, sexual selection, and sensory exploitation. Oxford Surveys in Evolutionary Biology 7:157-195.

2.  Ryan, M.J. 1994. Mechanistic studies in sexual selection. pp. 190-215. In: Real, L., editor, Behavioral Mechanisms in Evolutionary Ecology. University of Chicago Press, Chicago.

3.  Ryan, M.J.; Autumn, K,; Wake, D.B. 1998. Integrative biology and sexual selection. Integrative Biology 1:68-72.

4.  Ryan, M.J. 1991. Sexual selection and communication in frogs: some recent advances. Trends in Ecology and Evolution 6:351-354.

5.  Witte, K.; Ryan, M.J.; Wilczynski, W. in press. Changes in the frequency structure of a mating call decrease its attractiveness to females in the cricket frog Acris crepitans blanchardi. Ethology.

6.  Ryan, M.J. 1985. The Túngara Frog, A Study in Sexual Selection and Communication. University of Chicago Press, Chicago. 230 pp.

7.  Rand, A.S.; Ryan, M.J. 1981. The adaptive significance of a complex vocal repertoire in a Neotropical frog. Zeitschrift fur Tierpsychologie 57:209214.

8.  Ryan, M.J. 1980. Female mate choice in a Neotropical frog. Science 209:523525.

9.  Ryan, M.J. 1983. Sexual selection and communication in a Neotropical frog, Physalaemus pustulosus. Evolution 39:261272.

10.  Ryan, M.J.; Tuttle, M.D.; Taft, L.K. 1981. The costs and benefits of frog chorusing behavior. Behavioral Ecology and Sociobiology 8:273278.

11.  Tuttle, M. D.; Ryan, M.J. 1981. Bat predation and the evolution of frog vocalizations in the Neotropics. Science 214:677678.

12.  Ryan, M.J.; Tuttle, M.D.; Rand, A.S. 1982. Sexual advertisement and bat predation in a Neotropical frog. American Naturalist 119:136139.

13.  Bucher, T.L.; Ryan, M.J.; Bartholomew, G.W. 1982. Oxygen consumption during resting, calling and nest building in the frog Physalaemus pustulosus. Physiological Zoology 55:1022.

14.  Ryan, M.J.; Bartholomew, G.W.; Rand, A.S. 1983. Reproductive energetics of a Neotropical frog, Physalaemus pustulosus. Ecology 64:14561462.

15.  Ryan, M.J. 1985. Energetic efficiency of vocalization by the frog Physalaemus pustulosus. Journal of Experimental Biology 116:4752.

16.  Ryan, M.J. 1988. Energy, calling, and selection. American Zoologist 28:885-898.

17.  Ryan, M.J.; Rand. A.S. 1999. Phylogenetic inference and the evolution of communication in túngara frogs. pp. 535-557. In: Hauser, M.; Konishi, M. editors, The Design of Animal Communication. MIT Press, Cambridge, MA.

18.  Ryan, M.J.; Rand. A.S. 2001. Feature weighting in signal recognition and discrimination by the túngara frog. Pp. 86-101. In: Ryan, M.J. editor, Anuran Communication. Smithsonian Institution Press, Washington D.C.

19.  Ryan, M.J. 1986. Neuroanatomy influences speciation rates among anurans. Proceedings of the National Academy of Sciences 83:13791382.

20.  Ryan, M.J. 1998. Receiver biases, sexual selection and the evolution of sex differences. Science. 281:1999-2003.

21.  Ryan, M.J.; Phelps S.M.; Rand A.S. 2001. How evolutionary history shapes recognition mechanisms. Trends in Cognitive Science 5:143-148.

22.  Ryan, M.J.; Wilczynski, W. 1988. Coevolution of sender and receiver: effect on local mate preference in cricket frogs. Science 240:1786-1788.

23.  Ryan, M.J.; Perrill, S.A.; Wilczynski, W. 1992. Auditory tuning and call frequency predict population-based mating preferences in the cricket frog, Acris crepitans. American Naturalist 139:1370-1383.

24.  Keddy-Hector, A.; Wilczynski, W.; Ryan, M.J. 1992. Call patterns and basilar papilla tuning in cricket frogs. II. Intrapopulational variation and allometry. Brain, Behavior and Evolution 39:238-246.

25.  Wilczynski, W.; Keddy-Hector, A.; Ryan, M.J. 1992. Call patterns and basilar papilla tuning in cricket frogs. I. Differences among populations and between sexes. Brain, Behavior and Evolution 39:229-237.

26.  Sun, L.; Wilczynski, W.; Rand, A.S; Ryan, M.J. 2000. Trade-off in short and long distance communication in túngara (Physalaemus pustulosus) and cricket (Acris crepitans) frogs. Behavioral Ecology 11:102-109.

27.  Ryan, M.J.; Fox, J.H.; Wilczynski, W.; Rand, A.S. 1990. Sexual selection for sensory exploitation in the frog Physalaemus pustulosus. Nature 343:66-67.

28.  Ryan, M.J.; Rand, A.S. 1990. The sensory basis of sexual selection for complex calls in the túngara frog, Physalaemus pustulosus (sexual selection for sensory exploitation). Evolution 44:305-314.

29.  Rand, A.S.; Ryan, M.J.; Wilczynski, W. 1992. Signal redundancy and receiver permissiveness in acoustic mate recognition by the túngara frog, Physalaemus pustulosus. American Zoologist 32:81-90.

30.  Wilczynski, W.; Rand, A.S.; Ryan, M.J. 1995. The processing of spectral cues by the call analysis system of the túngara frog, Physalaemus pustulosus. Animal Behaviour 49:911-929.

31.  Ryan, M.J. 1996. Phylogenetics and behavior: some cautions and expectations. pp. 1-21. In: Martins, E. editor, Phylogenies and the Comparative Method in Animal Behavior. Oxford University Press, Oxford.

32.  Ryan, M.J. 1988. Constraints and patterns in the evolution of anuran acoustic communication. In: B. Fritzsch, M. Ryan, W. Wilczynski, W. Walkowiak, T. Hetherington, editors, The Evolution of the Amphibian Auditory System. pp.637-677. John Wiley and Sons Inc., New York.

33.  Cannatella, D.C.; Hillis, D.M.; Chippinendale, P.; Weigt, L.; Rand, A.S.; Ryan M.J. 1998. Phylogeny of frogs of the Physalaemus pustulosus species group, with an examination of data incongruence. Systematic Biology 47:311-335.

34.  Ryan, M.J. 1990. Signals, species, and sexual selection. American Scientist 78:46-52.

35.  Ryan, M.J.; Rand, A.S. 1993. Phylogenetic patterns of behavioral mate recognition systems in the Physalaemus pustulosus species group (Anura: Leptodactylidae): the role of ancestral and derived characters and sensory exploitation. pp. 251-267. In: D.R. Lees, D. Edwards, editors, Evolutionary Patterns and Processes. Linnean Society Symposium Series, No. 14, Academic Press, London.

36.  Ryan, M.J.; Rand, A.S. 1995. Female responses to ancestral advertisement calls in the túngara frog. Science 269, 390-392.

37.  Ryan, M.J.; Rand. A.S. 1999. Phylogenetic influences on mating call preferences in female túngara frogs (Physalaemus pustulosus). Animal Behaviour 57:945-956.

38.  Phelps, S.M.; Ryan, M.J. 1998. Neural networks predict response biases in female túngara frogs. Proceeding of the Royal Society, London series B 265:279-285.

39.  Phelps, S.M.; Ryan, M.J. 2000. History influences signal recognition: Neural network models of túngara frogs. Proceedings of the Royal Society, London series B 267:1633-1639.