An ethology reading list

At a meeting in New York last week [edit: many months ago by the time I got around to posting this], we were discussing the recent push in neuroscience for more naturalistic behaviors. One of the problems, someone pointed out, is that they are difficult to analyze. But surely there must be whole fields devoted to understanding natural behaviors? Why do we, as neuroscientists, not interact with them?

When I started this blog I named it neuroecology for exactly that reason: there was this whole field of ecology that has thought about natural behaviors very deeply for a long, long time and going over those papers on a blog seemed like a great way to understand them. What I didn’t understand at the time was that I was using the wrong word; it wasn’t ecology that I was looking for it was ethologyEcology is more generally about broad interactions between animals and environments. Ethology is the specific study of animal behavior.

So: ethologists. The studiers of natural animal behavior. What can neuroscientists learn from these mythical beings? I tried to collect as many syllabi as I could find (1, 2, 3, 4, 5, 6,  with thanks to Bence Ölveczky for sending me theirs in personal communication) to find papers that neuroscientists will find relevant for understanding how to analyze natural behaviors (with a few that I think are relevant thrown into the mix).

Consider this post a “living document” that I will update over time. Mostly it is a big list of papers that I have separated into sub-topics that drastically need to be cleaned up. If I’m missing something, let me know!

“Historically, different approaches to animal behavior were considered in Europe and the USA. Whereas European scientists, such as the winners of the 1972 Nobel prize for medicine or physiology, Lorenz, Tinbergen, and von Frisch, generally were concerned with the study of the behavior of animals in their natural environment. Indeed, the term ethology can be defined as the study of animals in their natural environment. By contrast, American scientists working with animal behavior generally performed experiments in controlled environments (e.g. a laboratory). This field of research is termed comparative psychology. Both approaches have advantages and disadvantages: The controlled experiments carried out within comparative psychology allow more rigour than the observational activities of ethologists, but the behaviors considered in such experiments may, on the other hand, differ strongly from the behaviors exhibited by animals in their natural environment.”

Some good (visual) examples in Approaches To Studying Animal Behavior (pdf)

Releasing Stimuli and Instinctive Behaviors

Tinbergen and Perdeck, On the stimulus situation releasing the begging response in the newly hatched herring gull chick (Larus agentatus agentatus pont). Behavior 3:1-39, 1950

Isogai, …, Dulac. Multisensory Logic of Infant-Directed Aggression by Males

Tinbergen and van Iersel, “Displacement reactions” in the three-spined stickleback. Behavior, 1:56-63, 1947

Lehrman, A critique of Konrad Lorenz’s theory of instinctive behavior. Quarterly Rev. Biol. 28:337-362, 1953

Tinbergen, N. On aims and methods of ethology. Zeitschrift f¨ur Tierpsychologie 20, 410-433 (1963).

Skinner, B. F. The experimental analysis of operant behavior. Annals of the New York Academy of Sciences 291, 374-385 (1977).

Leshner, A. & Pfaff, D. W. Quantification of behavior. PNAS 108 Supp 3, 15537-15541 (2011).

Chiel, H. J. & Beer, R. D. The brain has a body: adaptive behavior emerges from interactions of nervous system, body and environment. Trends Neurosci 20, 553-557 (1997).

Tinbergen, N. (1963). “On aims and methods of Ethology.” Zeitschrift fur tierpsychologie 20: 410-433.
At least one of the following 4 papers ::: DISCUSSION QUESTIONS
Dewsbury, D. A. (1992). “On the Problems Studied in Ethology, Comparative Psychology, and Animal Behavior.” Ethology 92(2): 89-107.
Alcock, J. and P. Sherman (1994). “The Utility of the Proximate-Ultimate Dichotomy in Ethology.” Ethology 96(1): 58-62.
Thierry, B. (2005). “Integrating proximate and ultimate causation: Just one more go!” Current Science 89(7): 1180-1183.
Dewsbury, D. A. (1999). “The proximate and the ultimate: past, present, and future.” Behavioural Processes 46(3): 189-199.

Swaisgood, R. R. and D. J. Shepherdson (2005). “Scientific approaches to enrichment and stereotypies in zoo animals: What’s been done and where should we go next?” Zoo Biology 24(6): 499-518.
Hosey, G. R. (1997). “Behavioural research in zoos: Academic perspectives.” Applied Animal Behaviour Science 51(3-4): 199-207.
Blumstein, D. and E. Fernandez-Juicic (2010). A Primer of Conservation Behavior, Sinaur. Chapter 1.

von Holst, E and U. St. Paul. 1960. On the functional
organization of drives

Models of behavior

Hydrodynamic, hierarchical, what else? Fixed action patterns.

– Dawkins, R. Hierarchical organisation: A candidate principle for ethology. (1976).

– Dawkins, R. & Dawkins, M. Hierarchical Organization and Postural Facilitation – Rules for Grooming in Flies. Animal Behaviour 24, 739-755 (1976). – Seeds, A. M. et al. A suppression hierarchy among competing motor programs drives sequential grooming in Drosophila. eLife 3, e02951 (2014).

Heiligenberg, W. Random processes describing the occurrence of behavioural patterns in a cichlid fish. Animal Behaviour 21, 169-182 (1973). – Stephens, G. J. et al. Emergence of long timescales and stereotyped behaviors in Caenorhabditis elegans. PNAS. 108, 7286-7289 (2011)

“The two models concerned are Lorenz’s ‘Hydraulic reservoir’4 and Tinbergen’s ‘Hierarchical system of centres ‘.5 Lorenz postulates for each instinctive act, a particular ‘reaction specific energy’ which he pictures as accumulating in a reservoir with a spring-valve at its base. In an appropriate stimulus situation, the spring-valve is released partly by the hydrostatic pressure of the reservoir’s contents and partly by the action of the external stimulus, which is pictureda weight on a scale pan pulling against the spring. Tinbergen, considering the total behaviour of the animal, uses a basically similar analogy when he speaks of’motivational impulses’ accumulating in ‘nervous centres’ where they are held in check by a ‘block’ which can be removed by an ‘innate releasing mechanism’ responsive to
particular external stimuli. The’ centres ‘ are supposed to be arranged in hierarchical systems each of which constitutes an ‘ instinct ‘. Lorenz’s model has been successful in accounting for many features of instinctive behaviour. For instance many instinctive responses are less easily evoked just after they have been performed-this is pictured by the emptying of the reservoir and the consequent reduction in hydrostatic pressure on the valve, so that a stronger external stimulus (weight on the scale pan) is necessary to release it again. Similarly the gradual increase in responsiveness with time since the previous performance is pictured as the gradual refilling of the reservoir. Tinbergen’s scheme provides in addition an opportunity for comprehending the organisation of large sections of the animal’s behaviour, and indicates the relations between the causal factors which govern it. These two models have thus played a fundamental r61e in the important recent advances in the study of animal behaviour for which Lorenz and Tinbergen have been mainly responsible.”

Quantifying behavior

Stephens, G. J. et al. Dimensionality and dynamics in the behavior of C. elegans. PLoS Comput Biol 4,
e1000028 (2008).
– Osborne, L. C. et al. A sensory source for motor variation. Nature 437, 412-416 (2005).

Berman, G. J. et al. Mapping the stereotyped behaviour of freely moving fruit flies. Journal of the Royal
Society Interface, 11, 20140672 (2014).
– Wiltschko, A. B. et al. Mapping Sub-Second Structure in Mouse Behavior. Neuron 88, 1121-1135 (2015).

Coen, P. et al. Dynamic sensory cues shape song structure in Drosophila. Nature 507, 233-237 (2014).

Porto, D. A. et al. Reverse-Correlation Analysis of Mechanosensation Circuit in C. elegans Reveals Temporal
and Spatial Encoding, bioRxiv (2017)

Sensory ecology

Endler, J. A. and A. L. Basolo (1998). “Sensory ecology, receiver biases and sexual selection.” Trends in Ecology & Evolution 13(10): 415-420.
Tobias, J. A., J. Aben, et al. (2010). “Song Divergence by Sensory Drive in Amazonian Birds.” Evolution 64(10): 2820-2839.
West, P. M. (2005). “The lion’s mane.” American Scientist 93(3): 226-235.
: Searcy, W. A. and S. Nowicki (2008). “Bird song and the problem of honest communication.” American Scientist 96(2): 114-121.

Lettvin, JY et al. 1959. What the frog’s eye tells the frogs brain.

Evolution

Oct 7 Andersson, M. and Y. Iwasa (1996). “Sexual selection.” Trends in Ecology & Evolution 11(2): A53-A58.
Eens, M. and R. Pinxten (2000). “Sex-role reversal in vertebrates: behavioural and endocrinological accounts.” Behavioural Processes 51(1-3): 135-147.
Andersson, M. and L. W. Simmons (2006). “Sexual selection and mate choice.” Trends in Ecology & Evolution 21(6): 296-302.
Clutton-Brock, T. (2007). “Sexual selection in males and females.” Science 318(5858): 1882-1885.
Gross, M. R. (1996). “Alternative reproductive strategies and tactics: Diversity within sexes.” Trends in Ecology & Evolution 11(2): 92-98.

Sapolsky, R. M. (2004). “Mothering style and methylation.” Nature Neuroscience 7(8): 791-792.
Weaver, I. C. G., N. Cervoni, et al. (2004). “Epigenetic programming by maternal behavior.” Nature Neuroscience 7(8): 847-854.
Nair, H. P. and L. J. Young (2006). “Vasopressin and pair-bond formation: Genes to brain to behavior.” Physiology 21: 146-152.

Ritschoff et al (2014) Neuromolecular responses to social challenge: Common mechanisms across mouse, stickleback fish, and honey bee. PNAS 111:17929–17934.
Pfennig et al (2014) Convergent transcriptional specializations in the brains of humans and song-learning birds. Science 346:1256846
FOR BACKGROUND O’Connell & Hofmann (2011) Genes, hormones, and circuits: An integrative approach to study the evolution of social behavior. Front. Neuroendo.

Bass, A. H. (1996). “Shaping brain sexuality.” American Scientist 84(4): 352-363. List as many hypotheses as you can, draw out the developmental timeline, refresh your memory on hormones.
Wingfiled et al (1987) “Testosterone and Aggression in Birds” Scientific American. List the 10 predictions of the challenge hypothesis.

(Organization of behavior?)

Aggression

Milinski (1987) TIT FOR TAT in sticklebacks and the evolution of cooperation Nature325, 433 – 435
Queller et al (2003) Single-gene green beard effects in the social amoeba Dictyostelium discoideum. Science 299:105-106
DuVal (2007) Cooperative display and lekking behavior of the Lance-tailed Manakin (Chiroxiphia Lanceolata. Auk 124:1168-1185
Smith, J. M. (1976). “Evolution and Theory of Games.” American Scientist 64(1): 41-45.
Mesterton-Gibbons, M. and E. S. Adams (1998). “Animal contests as evolutionary games.” American Scientist 86(4): 334-341.

Sapolsky (1990) Stress in the Wild. Scientific American Vol.262(1), p.106-113 (For Background)
Sapolsky (2005) The Influence of Social Heirarch and Primate Health Science. 308:648-652. (Newer paper similar to above For Background)
Tung et al (2012) Social environment is associated with gene regulatory variation in the rhesus macaque immune system. PNAS 109:6490-6495.

Foraging

Adams et al (2012) Neuroethology of decision-making. Curr Op in Neurobiol. 22:982–989
Stephens, D. W. (2008). “Decision ecology: Foraging and the ecology of animal decision making.” Cognitive Affective & Behavioral Neuroscience 8(4): 475-484.
Catania, K. C. and F. E. Remple (2005). “Asymptotic prey profitability drives star-nosed moles to the foraging speed limit.” Nature 433(7025): 519-522.

Moller, A. P. (2001). “Heritability of arrival date in a migratory bird.” Proceedings of the Royal Society of London Series B-Biological Sciences 268(1463): 203-206.
Lohmann, K. J. (1992). “How Sea-Turtles Navigate.” Scientific American 266(1): 100-106.
VanderLeest, H. T., T. Houben, et al. (2007). “Seasonal encoding by the circadian pacemaker of the SCN.” Current Biology 17(5): 468-473.

Individuality

Briffa, M. and A. Weiss (2010). “Animal personality.” Current Biology 20(21): R912-R914.
van Oers, K., P. J. Drent, et al. (2004). “Realized heritability and repeatability of risk-taking behaviour in relation to avian personalities.” Proceedings of the Royal Society of London Series B-Biological Sciences 271(1534): 65-73.
Sih, A., A. Bell, et al. (2004). “Behavioral syndromes: an ecological and evolutionary overview.” Trends in Ecology & Evolution 19(7): 372-378.

Endocrinology/peptides

Put in C. elegans stuff for sure

CPGs

Grillner S. 2003. The motor infrastructure: from ion channels to neuronal networks. Nat
Rev Neurosci 4:573–86.

Bagnall MW, McLean DL. 2014. Modular Organization of Axial Microcircuits in Zebrafish.
Science 343:197–200.

Josephson RK. 1985. Mechanical Power output from Striated Muscle during Cyclic
Contraction. J Exp Biol 114:493–512.

Gabaldón AM, Nelson FE, Roberts TJ. 2004. Mechanical function of two ankle extensors
in wild turkeys: shifts from energy production to energy absorption during incline versus
decline running. J Exp Biol 207:2277–88.

Akanyeti O, Putney J, Yanagitsuru YR, Lauder G V, Stewart WJ, Liao JC, Russell DW. 2017.
Accelerating fishes increase propulsive efficiency by modulating vortex ring geometry.
Proc Natl Acad Sci. doi: 10.1073/pnas.1705968115

Drucker EG, Lauder G V. 2000. A hydrodynamic analysis of fish swimming speed: wake
structure and locomotor force in slow and fast labriform swimmers. J Exp Biol
203:2379–93.

Ristroph L, Bergou AJ, Ristroph G, Coumes K, Berman GJ, Guckenheimer JM, Wang ZJ,
Cohen I. 2010. Discovering the flight autostabilizer of fruit flies by inducing aerial
stumbles. Proc Natl Acad Sci USA 107:4820–24.

Card, G. & Dickinson, M. Performance trade-offs in the flight initiation of Drosophila. J Exp Biol 211, 341-353
(2008).

Genetics

Weber, J. N., Peterson, B. K. & Hoekstra, H. E. Discrete genetic modules are responsible for complex burrow
evolution in Peromyscus mice. Nature 493, 402-405 (2013).
– Brown, A. E. X. et al. A dictionary of behavioral motifs reveals clusters of genes affecting Caenorhabditis
elegans locomotion. PNAS. 110, 791-796 (2013).

– Ayroles, J. F. et al. Behavioral idiosyncrasy reveals genetic control of phenotypic variability. PNAS 112,
6706-6711 (2015).
– Freund, J. et al. Emergence of Individuality in Genetically Identical Mice. Science 340, 756-759 (2013).

Social behavior

Vicsek, T. et al. Novel type of phase transition in a system of self-driven particles. Physical Review Letters
75, 1226-1229 (1995).
– Buhl, J. et al. From disorder to order in marching locusts. Science 312, 1402-1406 (2006).

– Couzin, I. D.et al. Effective leadership and decision-making in animal groups on the move. Nature 433,
513-516 (2005).
– Strandburg-Peshkin, A. et al. Shared decision-making drives collective movement in wild baboons. Science
348, 1358-1361 (2015).

Stress and the suppression of subordinate reproduction in cooperatively breeding meerkats

Prey Capture

Electric Fish Paper I: Detecting Object Distance
Electric Fish Paper II: Prey Capture
Von der Emde 1999
Von der Emde et al. 1998
Nelson & McIver 1999

Favorite Examples

Sound localization in Barn Owls (http://kernel.montana.edu/bioh430/readinglist.html)

Bat echolocation

Insect communication

Birdsong

Sober, S. J. & Brainard, M. S. Vocal learning is constrained by the statistics of sensorimotor experience. PNAS. 109, 21099-21103 (2012)

Primate communication

(Asif’s stuff)

Insect navigation

Chemotaxis

Olfaction

Other

Gepner, R., et al. Computations underlying Drosophila photo-taxis, odor-taxis, and multi-sensory integration. eLife 4, (2015)

Leave a Reply

Fill in your details below or click an icon to log in:

WordPress.com Logo

You are commenting using your WordPress.com account. Log Out /  Change )

Google photo

You are commenting using your Google account. Log Out /  Change )

Twitter picture

You are commenting using your Twitter account. Log Out /  Change )

Facebook photo

You are commenting using your Facebook account. Log Out /  Change )

Connecting to %s