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Earliest land tetrapods had problem swallowing

From: Ben Creisler

The new issue of Science has a short report of research presented at
the recent meeting of the  Society for Integrative and Comparative
Biology in San Francisco about the jaw and swallowing mechanisms of
early tetrapods:

Elizabeth Pennisi (2013)
Eating Was Tough For Early Tetrapods.
Science  339 (6118): 390-391
DOI: 10.1126/science.339.6118.390

While a fin-to-limb transition made possible the first steps on land
for vertebrates 390 million years ago, it took a long time for ancient
tetrapods to leave behind their aquatic ways and become true
landlubbers. After that initial landfall, another 80 million years
went by before tetrapods developed jaws adapted for terrestrial
feeding. Questions abound regarding the eating habits of early
tetrapods and how they were able to swallow.


The abstracts for the talks can be seen at:



Here are the texts of the abstracts:

S3-1. 2 ANDERSON, P*; FRIEDMAN, M; RUTA, M; Univ.  of Massachusetts,
Amherst, Univ.  of Oxford, UK, Univ.  of Lincoln,UK;

Diversity and disparity of the vertebrate feeding apparatus across the
invasion of land.

When vertebrates first colonized land, about 370 Mya, they encountered
a world full of new dietary resources requiring radical changes in
feeding mechanisms, not only at the water-land transition but also
within the terrestrial realm. However, recent work has indicated that
the earliest known limbed vertebrates had mechanical jaw systems
similar to their fish relatives.  Here, we extend the scope of initial
inquiries by examining the functional spectrum of feeding modes in a
diverse range of mostly Paleozoic, semi-terrestrial and terrestrial
early tetrapods.  We collected various biomechanically relevant
metrics from the lower jaws of a set of Devonian-Permian taxa:
stem-tetrapods (including fishes), stem-amphibians, stem-amniotes, and
crown-amniotes.  These data were used to construct  a morphofunctional
space illustrating the variety of biomechanical profiles explored by
these early tetrapods.  Relative disparity and morphospace occupation
across taxonomic groups and stratigraphic bins document a stepwise
occupation of various feeding guilds.  Interms of mechanical feeding
diversity, Devonian and Carboniferous stem tetrapods differ little
from lobe-finnedfishes.  It was not until the appearance of
Carboniferous and Permian stem amphibians and amniotes that terrestria
vertebrates began to expand into new regions of biomechanical
morphospace.  Our data support the hypothesis of a lag in the origin
of tetrapod herbivory; the first excursion into herbivore-guild space
does not occur until the latest Carboniferous.  These results suggest
that the conquest of land was a protracted event, lasting 80 My,
during which vertebrates developed the repertoire of jaw mechanics
necessary to fully exploit available terrestrial resources.


S3-2. 1 VAN WASSENBERGH, S. *; MICHEL, K. ; Univ. Antwerpen, Belgium;
sam. vanwassenbergh@ua. ac.be

Feeding and swallowing on land.

An important step towards understanding the evolution of
terrestriality in vertebrates is to identify how the aquatic ancestors
of tetrapods were able to access ground-based prey. Since several
extant lineages of bony fishes show an amphibious feeding lifestyle,
these fishes can be used to study the biomechanical requirements of
successful aquatic to terrestrial transitions to capture and transport
prey in their buccopharyngeal cavity.  We analyzed the functional
morphology and kinematics of two morphologically distinct and
distantly related species that are both successful terrestrial
feeders: the mudskipper (Periophthalmus barbarus) and theeel-catfish
(Channallabes apus).  During prey capture, themudskipper pivots over
its strong pectoral fins, and uses its complex system of oral jaws to
pick up pieces of food on land. Notably, we found that this species
still makes use of water carried along in the buccopharyngeal cavity
to assist prey capture, and to provide intra-oral transport of food
towards the esophagus by performing suction movements.  This mechanism
is markedly different from the eel-catfish, which curls into aposition
where the head is strongly bended ventrally, scans the surface by
moving its head and chemotactile barbels from side to side, and
performs a typical rostro-caudal wave of buccopharyngeal expansion of
the jaws, hyoid and opercular system (as in most suction feeding
fish).  These findings show that having weight-bearing pectoral fins
is not a prerequisite for capturing prey on land in a fish that has a
flexible body.  Unlike the mudskipper, the eel-catfish does not use a
hydrodynamic tongue to swallow the prey, but returns to the water to
perform the necessary food transport.  Consequently, these examples
show two clearly different strategies to overcome the problems imposed
by the shift from an aquatic to a terrestrial environment for feeding.


S3-1. 1 COATES, M.  I. ; Univ.  of Chicago, Chicago; mcoates@uchicago.edu

Vertebrate diversity and phylogeny across the fish-to-tetrapod transition.

The popular idea of the fish-to-tetrapod transition covers a series of
changes to the gnathostome body plan: mid-line fins are lost; digited
limbs replace paired fins; a sacrum links vertebrae to hips; gills are
reduced; a distinct neck separates the head from shoulders.  Such
changes (and many more) occur within taxa traditionally designated as
fish, deep within the tetrapod stem lineage.  Moreover, if
traditional, anatomical character-based definitions of taxa are used,
then the broad shape of tetrapod evolution resembles an ice-cream
cone: the classic spindle diagram.  A few proto-tetrapods exhibiting a
classic mosaic of fish- and tetrapod-like features emerge within the
Devonian Period some 380 million years ago, and these earliest forms
constitute a phylogenetic fuse preceding a dramatic evolutionary
radiation within the Mississippian(around 340 million years ago) from
which sprang the roots of modern amniotes and lissamphibians.
However, if the tetrapods are defined on the basis of all taxa more
closely related to living forms than to lungfishes (or coelacanths),
then the picture of  diversity flanking the fish-to-tetrapod
transition changes. Diverse and abundant Devonian tetrapods are cut
down by the end Devonian (360 million years ago) Hangenberg
extinction,the causes and consequences of which are only now being
investigated.  Modern vertebrate diversity, dominated by tetrapods,
teleosts and elasmobranchs, is contingent upon this event.  The
fish-to-tetrapod transition occurred within a very different and
earlier faunal setting, and begs questions about survivorship versus
extinction, recovery and replacement, and the extent to which the
phylogenetic pattern apparent among early tetrapods is repeated within
the other major vertebrate clades.


S3-1. 3 PIERCE, SP*; HUTCHINSON, JR; CLACK, JA; The RoyalVeterinary
College, UK, University Museum of Zoology,Cambridge, UK;

Historical evolution of early tetrapod movement.

Conceptualizations of the evolution of tetrapod locomotion have
changed drastically in the past 50 years.  When early tetrapod fossils
were first discovered, the animals were reconstructed as
salamander-like in their mode of locomotion, walking around on four
sturdy legs.  In fact, the "prototetrapod" was envisaged as a
terrestrially capable creature with a fish-like body and modified
pectoral/pelvic fins equipped with weight supporting joints and the
beginnings of digits, but no sacrum.  'Conquest of land' was seen as
the driving force in the evolution of limbs.  However,intensive
re-examination of fossil material and the discovery of key specimens
has gradually redefined our perception of the tetrapod bauplan.  The
prevailing theory is that early tetrapods were primarily aquatic in
habit and that limbs evolved before the ability to ‘walk’ on land.
New fossil footprints have challenged this idea by inferring early
tetrapods were walking -perhaps partially supported by water - 20
million years before any known tetrapod body fossils.  Another recent
study has posited that sarcopterygian fishes evolved hindlimb powered
locomotion, which was later exapted for usage in tetrapods. However,
our recent work on the late Devonian tetrapod Ichthyostega has
demonstrated that its limb joints did not permit a walking gait like
that of a living salamander, and that land locomotion was
forelimb-driven.  Considering that other closely related stem
tetrapods seem to have had a similar limb joint structure, this may
have been an ancestral state, although the anatomy of earlier Devonian
tetrapods remains unknown. The historical transformation of locomotion
potential, and the drivers of land dwelling in the earliest limbed
vertebrates, has thus changed drastically, with several different
hypotheses having been put forward over the past few years.  New
information and methodological techniques are helping to refine and
shape our understanding of this pivotal evolutionary event.


S3-1. 4 DAVIS, Marcus C; Kennesaw State University;mdavi144@kennesaw.edu

The deep homology of the tetrapod limb: Combining fossil and genetic datasets.

The evolution of tetrapod limbs from fish fins was a significant
functional shift.  But how significant was this shift in terms of
morphology and gene regulation? The fossil record provides insight
into the morphological changes.  However, to understand the underlying
mechanisms we must peer into the gene regulatory networks of living
vertebrates.  Until recently,data from gene expression and functional
studies in tetrapods and teleosts supported the notion that the distal
region of the tetrapod limb, the autopod (wrist, ankle, and digits),
was an evolutionary novelty.  In contrast, the fossil data suggests
that the autopod was already present in fish fins prior to the origin
of tetrapods, and was subsequently modified for new adaptive roles in
terrestrial locomotion, feeding, and support.  Data from
phylogenetically more basal extant taxa has helped to reconcile these
datasets.  Hox genes encode transcription factors that provide
positional identity along animal axes, including the axes of the
fins/limbs.  Our analysis of Hox expression in a basal
actinopterygian, the North American paddlefish, Polyodon spathula
reveals patterns of expression long considered to be developmental
hallmarks of the autopod and shown intetrapods to be controlled by a
‘digit enhancer’ regulatory region.  But we also observe differences:
For example, in Polyodon, early and late phases of HoxD expression
overlap proximodistally, whereas in tetrapods these phases are
spatially segregated.  These data demonstrate that aspects of Hox
expression once considered unique to autopods are, in fact, ancestral
to tetrapod limbs.  However, our data also show that tetrapod limbs
exhibit a unique regulatory context – different in key ways from the
fins of fish.  Together, these results suggest that novelty in the
tetrapod limb has arisen by changes in regulation of an ancient and
conserved pattern of gene expression.