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Evolution of mammal diving capacity



From: Ben Creisler
bcreisler@gmail.com

A new non-dino paper that may be of interest:

Scott Mirceta, Anthony V. Signore, Jennifer M. Burns, Andrew R.
Cossins, Kevin L. Campbell, Michael Berenbrink (2013)
Evolution of Mammalian Diving Capacity Traced by Myoglobin Net Surface Charge.
Science 340 (6138)
DOI: 10.1126/science.1234192
http://www.sciencemag.org/content/340/6138/1234192



Extended breath-hold endurance enables the exploitation of the aquatic
niche by numerous mammalian lineages and is accomplished by elevated
body oxygen stores and adaptations that promote their economical use.
However, little is known regarding the molecular and evolutionary
underpinnings of the high muscle myoglobin concentration phenotype of
divers. We used ancestral sequence reconstruction to trace the
evolution of this oxygen-storing protein across a 130-species
mammalian phylogeny and reveal an adaptive molecular signature of
elevated myoglobin net surface charge in diving species that is
mechanistically linked with maximal myoglobin concentration. This
observation provides insights into the tempo and routes to enhanced
dive capacity evolution within the ancestors of each major mammalian
aquatic lineage and infers amphibious ancestries of echidnas, moles,
hyraxes, and elephants, offering a fresh perspective on the evolution
of this iconic respiratory pigment.

===

Introduction

Evolution of extended breath-hold endurance enables the exploitation
of the aquatic niche by numerous mammalian lineages and is
accomplished by elevated body oxygen stores and morphological and
physiological adaptations that promote their economical use. High
muscle myoglobin concentrations in particular are mechanistically
linked with an extended dive capacity phenotype, yet little is known
regarding the molecular and biochemical underpinnings of this key
specialization. We modeled the evolutionary history of this
respiratory pigment over 200 million years of mammalian evolution to
elucidate the development of maximal diving capacity during the major
mammalian land-to-water transitions.

Evolutionary reconstruction of myoglobin net surface charge in
terrestrial and aquatic mammals. The figure reveals a molecular
signature of elevated myoglobin net surface charge in all lineages of
living elite mammalian divers with an extended aquatic history (upper
silhouettes). This signature is used here to infer the diving capacity
of extinct species representing stages during mammalian land-to-water
transitions (†).

Methods

We first determined the relationship between maximum myoglobin
concentration and its sequence-derived net surface charge across
living mammalian taxa. By using ancestral sequence reconstruction we
then traced myoglobin net surface charge across a 130-species
phylogeny to infer ancestral myoglobin muscle concentrations. Last, we
estimated maximum dive time in extinct transitional species on the
basis of the relationship of this variable with muscle myoglobin
concentration and body mass in extant diving mammals.

Results
We reveal an adaptive molecular signature of elevated myoglobin net
surface charge in all lineages of mammalian divers with an extended
aquatic history—from 16-g water shrews to 80,000-kg whales—that
correlates with exponential increases in muscle myoglobin
concentrations. Integration of this data with body mass predicts 82%
of maximal dive-time variation across all degrees of diving ability in
living mammals.


Discussion

We suggest that the convergent evolution of high myoglobin net surface
charge in mammalian divers increases intermolecular electrostatic
repulsion, permitting higher muscle oxygen storage capacities without
potentially deleterious self-association of the protein. Together with
fossil body-mass estimates, our evolutionary reconstruction permits
detailed assessments of maximal submergence times and potential
foraging ecologies of early transitional ancestors of cetaceans,
pinnipeds, and sea cows. Our findings support amphibious ancestries
for echidnas, talpid moles, hyraxes, and elephants, thereby not only
establishing the earliest land-to-water transition among placental
mammals but also providing a new perspective on the evolution of
myoglobin, arguably the best-known protein.