The evolution of lateralized foot use in parrots: a phylogenetic approach

Behavioral Ecology doi:10.1093/beheco/arr114 Advance Access publication 11 July 2011 Original Article The evolution of lateralized foot use in parrots: a phylogenetic approach Cerebral lateralization refers to the division of cognitive function in either brain hemisphere and may be overtly expressed as behavioral asymmetries, such as handedness. The evolutionary history of laterality is of considerable interest due to its close link with the development of human language. Although considerable research effort has aimed at the proximate explanations of cerebral lateralization, considerably less attention has been paid to ultimate explanations. The extent to which laterality is constrained by phylogeny or shaped by ecological forces through natural selection has received little attention. Here, the foot preference of 23 species of Australian parrots was examined to investigate the link between laterality and body size. The raw data indicated that the strength of laterality was related to body size and an associated foraging mode. The results of the phylogenetic generalized least squares, however, indicated that both the pattern (left, right, or ambidextrous) and strength of laterality showed a high degree of phylogenetic inertia. Regressions based on independent contrasts revealed no relationship between laterality and body size. These results suggest that laterality in Australian parrots has been shaped by just a few events deep in their evolutionary history. We hypothesize that cerebral lateralization may provide a fitness benefit to larger bodied species that extract seeds from seedpods using coordinated foot–beak actions. The secondary loss of laterality in smaller body species may have been associated with a shift to grazing on small seeds and blossoms as Australia became increasingly arid. Key words: behavior, ecology, foraging, laterality, lateralization, phylogeny. [Behav Ecol 22:1201–1208 (2011)] INTRODUCTION erebral lateralization (the division of cognitive processing between the 2 brain hemispheres) was considered a unique human trait for over a century because of its intimate relationship with the control of human speech and other ‘‘higher order’’ cognitive functions (Crow et al. 1998; Rogers 2000; Corballis 2002). Recent studies on lateralization of cognitive function have shown that it is in fact a ubiquitous vertebrate trait and may be common even among invertebrates (Vallortigara 2000; Byrne et al. 2002; Rogers and Vallortigara 2008). Cerebral lateralization is often expressed behaviorally and behavioral side baises that it produces are collectively referred to as laterality. Domestic chicks, for example, have a left-sided turning bias (Casey and Karpinski 1999), toads use the right paw to wipe objects from their head (Bisazza et al. 1996), and a number of parrot species favor the left or right foot to manipulate objects (Rogers 1980; Magat and Brown 2009). Cerebral lateralization, therefore, is most likely an ancient evolutionary trait that has a substantial influence on behavioral expression in animals and provides a noninvasive insight into the workings of the animal mind. Several lines of evidence suggest that laterality plays an important role in shaping the everyday behavior of animals and is subject to natural selection (Vallortigara and Rogers 2005). Firstly, there is ample evidence that laterality varies between individuals within populations. For example, individ- C Address correspondence to C. Brown. E-mail: culum.brown@mq. edu.au. M.M. Coauthor is now at Centre for Vascular Research, The University of Sydney, Sydney, NSW 2006, Australia Received 2 March 2011; revised 5 May 2011; accepted 25 May 2011.
The Author 2011. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: ual chimps show different hand preferences while fishing for termites and strongly lateralized individuals are more efficient at extracting termites than ambidextrous individuals irrespective which hand they use (Marchant and McGrew 1996). Secondly, variation in laterality has fitness consequences; strongly lateralized parrots are better able to solve novel problems than nonlateralized parrots (Magat and Brown 2009). Similarly, schools comprised of strongly lateralized fish are more highly synchronized then schools of nonlateralized fish (Bisazza and Dadda 2005). Lastly, lines of strongly and leftand right-biased fish populations have been produced in the laboratory by artificial selection thus, in fish at least, laterality is partially heritable (Bisazza et al. 2000; Brown et al. 2007). Moreover, comparative data collected from fish populations that differ in their exposure to predation pressure reveal population level variation in laterality (Brown et al. 2004). Thus, there is also some evidence of evolution acting to shape lateralized characters in wild populations. If laterality is favored by natural selection as illustrated above, it raises the intriguing question as to why we see so much variation at both the individual and species levels. Put simply, why are not all animals strongly lateralized? Some species of parrots contain left, right footed, and ambidextrous individuals approximating a normal distribution at the species level. In other species, however, the population distribution is strongly skewed with all individuals being strongly left footed, whereas in still other species, all individuals are strongly right footed (Brown and Magat 2011). This conundrum has received considerable attention in reviews addressing various factors that might contribute to population level biases in laterality (see e.g., Vallortigara and Rogers 2005; Corballis 2009; Ghirlanda et al. 2009). More generally, the lack of uniformity within species and across closely related species suggests that laterality must also incur costs that are likely to be context specific. Experimental work on fishes has shown that Culum Brown and Maria Magat Department of Biological Sciences, Macquarie University, Sydney, NSW 2109, Australia Behavioral Ecology 1202 history. When taken together with ecological data, one can elucidate the likely evolutionary forces that may have shaped the distribution of the trait over time. Australian parrots occupy a wide range of habitats and feed on a variety of different food sources, some requiring manipulation with the foot (e.g., large banksia seedpods), whereas others do not (e.g., small grass seeds and nectar). Thus, we can use parrots as a model family to examine the link between foraging ecology and the evolution of lateralization. The preferential use of the left or right foot, however, may also be constrained by phylogeny whereby closely related species should show evidence of niche conservatism (i.e., identity by descent). In the latter case, we would expect to see consistent foot preferences within each of the major parrot clades, whereas in the f (...truncated)