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Edited by Nicholas D. Pyenson, Smithsonian Institution, Washington, DC, and accepted by Editorial Board Member David Jablonski February 23, 2018 (received for review August 8, 2017)
Significance
The reasons why aquatic mammals exhibit larger average sizes than their terrestrial relatives have long been debated. Most previous hypotheses have focused on releases from terrestrial constraints on large sizes. Through the analysis of mammal size distributions, we find the aquatic realm imposes stronger constraints on body size than does the terrestrial realm, driving and confining aquatic mammals to larger sizes. Calculations of energy intake and demand as a function of body size indicate heat loss imposes a strong lower bound on size, whereas the scaling of feeding rate versus metabolic rate imposes a constraint on maximum size. Rather than freeing animals from body size constraints, living in water appears to impose stronger selective pressures than does living on land.
Abstract
Four extant lineages of mammals have invaded and diversified in the water: Sirenia, Cetacea, Pinnipedia, and Lutrinae. Most of these aquatic clades are larger bodied, on average, than their closest land-dwelling relatives, but the extent to which potential ecological, biomechanical, and physiological controls contributed to this pattern remains untested quantitatively. Here, we use previously published data on the body masses of 3,859 living and 2,999 fossil mammal species to examine the evolutionary trajectories of body size in aquatic mammals through both comparative phylogenetic analysis and examination of the fossil record. Both methods indicate that the evolution of an aquatic lifestyle is driving three of the four extant aquatic mammal clades toward a size attractor at ∼500 kg. The existence of this body size attractor and the relatively rapid selection toward, and limited deviation from, this attractor rule out most hypothesized drivers of size increase. These three independent body size increases and a shared aquatic optimum size are consistent with control by differences in the scaling of energetic intake and cost functions with body size between the terrestrial and aquatic realms. Under this energetic model, thermoregulatory costs constrain minimum size, whereas limitations on feeding efficiency constrain maximum size. The optimum size occurs at an intermediate value where thermoregulatory costs are low but feeding efficiency remains high. Rather than being released from size pressures, water-dwelling mammals are driven and confined to larger body sizes by the strict energetic demands of the aquatic medium.
Footnotes
- ↵1To whom correspondence should be addressed. Email: wgearty{at}stanford.edu.
Author contributions: W.G., C.R.M., and J.L.P. designed research; W.G. performed research; W.G. analyzed data; and W.G., C.R.M., and J.L.P. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission. N.D.P. is a guest editor invited by the Editorial Board.
Data deposition: The code and data for all analyses are available at BitBucket (https://bitbucket.org/wgearty/body-size-analyses/).
See Commentary on page 3995.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1712629115/-/DCSupplemental.
Published under the PNAS license.
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Energetic tradeoffs control the size distribution of aquatic mammals
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- Biological Sciences
- Evolution
- Physical Sciences
- Earth, Atmospheric, and Planetary Sciences
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