Running for life: How speed restricts evolutionary change of the vertebral column

One of the riddles of mammal evolution explained: the strong conservation of the number of trunk vertebrae. Researchers of the Naturalis Biodiversity Center and the University of Utah show that this conservation is probably due to the essential role of speed and agility in survival of fast running mammals. They measured variation in vertebrae of 774 individual mammal skeletons of both fast and slow running species. The researchers found that a combination of developmental and biomechanical problems prevents evolutionary change in the number of trunk vertebrae in fast running and agile mammals. In contrast, these problems barely affect slow and sturdy mammals. The study will appear next Monday, 14 July 2014 in PNAS.

The mammal vertebral column is highly variable among species, reflecting adaptations to a wide range of lifestyles, from burrowing in moles to flying in bats. Yet, as a rule, the number of trunk vertebrae varies little between most mammal species. The vertebral column and its high evolutionary potential is considered to be of central importance for the evolution of vertebrates, which is why the constancy is both puzzling and important. The authors propose, on biomechanical and developmental grounds that evolutionary change is virtually impossible in fast running and agile mammals, but only marginally affects slow and sturdy mammals. The rationale is that several mutations are necessary to change the number of trunk vertebrae, with single mutations leading to irregularly shaped transitional lumbosacral vertebrae that are incompletely and asymmetrically fused to the sacrum. These irregular lumbosacral joints reduce flexibility, thus severely hampering running and jumping. Their observations indeed show that selection against these initial changes is strong in fast and agile mammals and weak in slower and sturdier ones.

In total, 774 skeletons of 90 different species were analysed. The skeletons belonged to collections of 9 European natural history museums including Naturalis Biodiversity Center, Leiden.

"The stiffness of the back of a mammal is key to whether evolutionary change is possible or not", said Frietson Galis, one of the authors of the study. "`the locomotion of slow mammals with a stiff back is only marginally affected by irregular lumbosacral joints, but for fast running mammals such joints are fatal " continued Clara ten Broek another author of the study.

"A combination of developmental, biomechanical and evolutionary insights and a large dataset were necessary to solve this puzzle of mammal evolution", said Frietson Galis.

"The stiffness of the back of a mammal is key to whether evolutionary change is possible or not", said Frietson Galis, researcher at Naturalis Biodiversity Center and one of the authors of the study. "the locomotion of slow mammals with a stiff back is only marginally affected by irregular lumbosacral joints, but for fast running mammals such joints are fatal" continued Clara ten Broek another author of the study.

"A combination of developmental, biomechanical and evolutionary insights and a large dataset were necessary to solve this puzzle of mammal evolution", said Frietson Galis.

Images:

Photographs 1A and 1B

Title: Skeletons of a slow and sturdy elephant (1A) and of a fast and flexible Dorcas gazelle (1B).

Caption: (1A) Skeleton of a juvenile specimen of an Asian elephant with a stiff vertebral column, due to the long thorax with many ribs, the short lumbar ribless region (behind the thorax) and the dorsal spines that are all backward pointing. (1B) Skeleton of a Thomson's gazella with a flexible vertebral column, due to the short thorax, long lumbar region and the dorsal spines that are anteriorly backward pointing and posteriorly forward pointing, allowing dorsal flexion of the spine. Photo: Joris van Alphen / jorisvanalphen.com.

Licence for photo use: these photographs may freely be used in print and electronic publications about this PNAS study, provided that proper attribution to the photographer is made. For more photos and any other kind of use, contact Joris van Alphen (joris@jorisvanalphen.com, or tel. +31647554525).

Photograph 2

Title: Authors Frietson Galis (left) and Clara ten Broek investigating the vertebral column of a Thomson's gazelle. Photo: Eelco Kruidenier, © Naturalis.

Licence for photo use: This photograph may freely be used in print and electronic publications about this PNAS study, provided that proper attribution to the photographer is made.

Citation to the article: Frietson Galis, David R. Carrier, Joris van Alphen, Steven D. van der Mije, Tom J.M. Van Dooren, Johan A. J. Metz, Clara M.A. ten Broek 2014. Fast running restricts evolutionary change of the vertebral column in mammals. Proc. Natl. Acad. Sci. USA, http://www.pnas.org/cgi/doi/10.1073/pnas.1401392111

Media contacts:

For the authors: Frietson Galis, frietson.galis@naturalis.nl, Phone: +316 48814360

For Naturalis: Rebecca Reurslag, Rebecca.reurslag@naturalis.nl, Phone: +3171 56 87 625

For PNAS: PNAS News Office at pnasnews@nas.edu, Phone: +1 202-334-1310

Abstract of the article:

The mammalian vertebral column is highly variable, reflecting adaptations to a wide range of lifestyles, from burrowing in moles to flying in bats. Yet, in many taxa the number of trunk vertebrae is surprisingly constant. We argue that the latter constancy results from strong selection against initial changes of these numbers in fast-running or agile mammals, while such selection is weak in slower-running, sturdier mammals. The rationale is that changes of the number of trunk vertebrae require homeotic transformations from trunk into sacral vertebrae, or vice versa, and mutations towards such transformations generally produce transitional lumbosacral vertebrae that are incompletely fused to the sacrum. We hypothesize that such incomplete homeotic transformations impair flexibility of the lumbosacral joint and, thereby threaten survival in species that depend on axial mobility for speed and agility. Such transformations will only marginally affect performance in slow sturdy species, so that sufficient individuals with transitional vertebrae survive to allow eventual evolutionary changes of trunk vertebral numbers. We present data on fast and slow carnivores and artiodactyls and on slow afrotherians and monotremes that strongly support this hypothesis. The conclusion is that the selective constraints on the number of trunk vertebrae stem from a combination of developmental and biomechanical constraints.

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