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
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Ryan, M.J. 1990. Sensory systems, sexual selection, and sensory exploitation. Oxford Surveys in
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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.
Ryan, M.J.; Autumn, K,; Wake, D.B. 1998. Integrative biology and sexual selection. Integrative
Biology 1:68-72.
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.
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Ryan, M.J. 1983. Sexual selection and communication in a Neotropical frog, Physalaemus
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