On the origin of skilled forelimb movements

doi:10.1016/S0166-2236(00)01618-0

Trends in Neurosciences

Volume 23, Issue 8, 1 August 2000, Pages 372-376

https://doi.org/10.1016/S0166-2236(00)01618-0 Get rights and content

Abstract

Homologizing behaviour was once considered unreliable, but the application of modern comparative methods has been shown to provide strong evidence of behavioural homologies. Skilled forelimb movements were thought to originate in the primate lineage but in fact are common among tetrapod taxa and probably share a common origin in early tetrapods. Furthermore, skilled movements are likely to have been derived from, and elaborated through, food-handling behaviour. In addition, it is now thought that the role played by the lateral and medial descending pathways of the spinal cord in the execution of skilled forelimb movements could be synergistic, rather than the exclusive responsibility of an individual pathway.

Section snippets

Homoplasy or homology?

The question of homoplasy or homology is complex because there is considerable debate regarding what constitutes a homologous trait18, 19. For the purposes of the present analysis, we have treated skilled forelimb movements as homologous if they can be continuously traced back to a common ancestor²⁰ by mapping the presence of skilled forelimb movements on top of a phylogeny. This definition has been used in both behavioural²¹ and neural²² studies. By mapping the given traits onto a known

Character mapping and ancestral state reconstruction

A phylogeny of the various groups was reconstructed on the basis of a variety of recent studies on tetrapod evolution31, 32, 33, 34. Although the arrangement of some taxa might be questionable, it is important to note that different arrangements35, 36, 37 gave the same results.

Several different algorithms can be used to determine the most likely ancestral states of reconstructed characters38, 39, 40. Two different methods were employed: maximum parsimony and unequal gains and losses. Maximum

Tracing the evolution of skilled forelimb movements

Mapping of skilled forelimb movements using maximum parsimony yielded an ancestral state of 0 for the base of the tree (Fig. 2). That is, the presence of skilled forelimb movements was absent at the base of the tetrapod phylogeny. Similarly, the bases of the Amphibia, the Reptilia and the Mammalia indicate a lack of skilled forelimb movements. Skilled forelimb movements are found in ancestral therian mammals (the marsupials and all other non-egg-laying mammals) after the branching of the

Where did skilled forelimb movements come from?

The present analysis suggests that skilled forelimb movements are an ‘ancestral’ feature of mammals, and possibly tetrapods, that has its origins relatively early in evolutionary history. One intriguing question that arises from this analysis is what are skilled forelimb movements derived from? Previous investigations have suggested that they are derived from digging behaviour⁸ or locomotion⁴³. However, a close examination of frog forelimb movements involved in reaching and grasping prey

Neural control of skilled forelimb movements

Skilled forelimb movements appear to have originated early in tetrapod evolution, possibly as early as the divergence between amphibians and amniotes. This implies that various aspects of the nervous system that have traditionally been considered to be integral to the execution of skilled forelimb movements are not required. For example, the corticospinal tract (CST) has been suggested to be a crucial descending pathway from the brain, coordinating the execution of skilled forelimb movements12,

Concluding remarks

Although the consistency of the data is suggestive of an ancestral origin of skilled forelimb movements, more research needs to be focused upon forelimb usage in non-mammalian vertebrates to give greater confidence to these results. In particular, detailed studies of forelimb use in lizards could yield insight into the neural substrates responsible for the execution of skilled forelimb movements. Once suitable data has been obtained for lizards and lesser-studied mammalian taxa, we might be

Acknowledgements

The authors thank the helpful staff of the following zoological parks for allowing us to observe the animals under their care: Assiniboine Park Zoo, Calgary Zoo, Los Angeles County Zoo, Melbourne Zoo, Milwaukee County Zoo, Mountain View Breeding Farms, Oaklawn Farm Zoo, Paris Zoo, Shubenacadie Wildlife Park and Valley Zoo. They also thank Lucie Gray and Kiisa Nishikawa for sending a copy of their frog footage, Gordon Burghardt for discussions on saurid and chelonian ethology, and Sergio Pellis

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Cited by (190)

Reaching an understanding of cortico-medullary control of forelimb behaviors
2023, Cell
Structural and functional map for forelimb movement phases between cortex and medulla
2023, Cell
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2021, Behavioural Brain Research
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2023, bioRxiv
Online repositories of photographs and videos provide insights into the evolution of skilled hindlimb movements in birds
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Cortical Network and Projection Neuron Types that Articulate Serial Order in a Skilled Motor Behavior
2023, SSRN

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Trends in Neurosciences

ReviewOn the origin of skilled forelimb movements

Abstract

Section snippets

Homoplasy or homology?

Character mapping and ancestral state reconstruction

Tracing the evolution of skilled forelimb movements

Where did skilled forelimb movements come from?

Neural control of skilled forelimb movements

Concluding remarks

Acknowledgements

Behav. Brain Res.

Behav. Brain Res.

Behav. Brain Res.

Behav. Brain Res.

Curr. Opin. Neurobiol.

Mol. Phylogenet. Evol.

Trends Ecol. Evol.

Behav. Brain Res.

Behav. Brain Res.

Behav. Brain Res.

Neurosci. Res.

Behav. Brain Res.

Grasping in modern primates: the evolutionary context

Studies of the hands of living primates

Proc. Zool. Soc. London

Brain size is not correlated with forelimb dexterity in fissiped carnivores (Carnivora): a comparative test of the principle of proper mass

Brain Behav. Evol.

The relationships between brain regions and forelimb dexterity in marsupials (Marsupialia): a comparative test of the principle of proper mass

Aust. J. Zool.

Evolution of forelimb movement patterns for prey manipulation in Anurans

J. Exp. Zool.

The Pyramidal Tract

Evolutionary Biology

The role of the corticospinal tract in the evolution of human digital dexterity

Brain Behav. Evol.

Variation in form of the corticospinal tract and its relationship to digital dexterity

Brain Behav. Evol.

Evolution of the Brain: Creation of the Self

Carnivore brain size, behavioral ecology, and phylogeny

J. Mammal.

Relative brain size and behavior in archosaurian reptiles

Annu. Rev. Ecol. Syst.

Review
On the origin of skilled forelimb movements