G404 Geobiology
Evolution of the Skeleton
Reading Benton Chapter 5
The Vertebrate Archetype (Richard Owen)
Department of Geological Sciences | Indiana University
(c) 2011, P. David Polly
G404 Geobiology
Next week
Tuesday (17 Sept): Paper Discussion
Purnell, M. A. 2001. Scenarios, selection and the ecology of early vertebrates. Pp. 187-208 in P. E.
Ahlberg (ed.), Major Events in Vertebrate Evolution: Palaeontology, Phylogeny, Genetics, and
Development. Palaeontological Association Special Volume Series, 61. Taylor and Francis: London.
Wednesday (18 Sept): No formal lab
You may visit the Zooarchaeology Collection during lab hours. Let Ryan
Kennedy know as a courtesy if you plan on going ([email protected]).
Thursday (19 Sept): No lecture
Tuesday (24 Sept): Midterm I, Project proposal due
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•
•
•
be able to fully label diagrams of dermatocranium and amniote skeleton
be familiar with terms listed in Lab 1 handout
be familiar with modern tetrapod groups and their phylogenetic relationships
be familiar with the Carboniferous Crisis and its relevance to vertebrate evolution (first lecture, see
reference by Sahney et al if you want to read more)
• be familiar with the homology and evolution material from today’s lecture
• be familiar with chordate characters and early fossil chordates
Department of Geological Sciences | Indiana University
(c) 2011, P. David Polly
G404 Geobiology
Schematic view of two aspects of evolution
Aspect 1: evolutionary change. involves change in a species’ (populations’)
average morphology and variation around that mean over time. Results in
morphological change.
Aspect 2: speciation. involves splitting of a species from one population into
more than one. Results in increased diversity (where diversity means number
of species).
Descendant B
Time
Descendant A
Speciation event
Ancestor
Morphology
(e.g., big tabular versus small tabular)
Department of Geological Sciences | Indiana University
(c) 2011, P. David Polly
G404 Geobiology
Two definitions of species
Biological species definition: “Species is a population of interbreeding
individuals reproductively isolated from other such populations” (after Mayr, 1942)
• emphasizes the fact that there is variation within species
• emphasizes that the only way for species to become different is when they
are reproductively isolated
• emphasizes that speciation requires the breakdown of gene flow for two
isolated populations to emerge
Evolutionary species definition: “Species is a lineage (ancestor-descendant
sequence of populations) evolving separately from others with its own
tendencies” (after Simpson, 1961)
• emphasizes role of reproductive isolation in speciation
• emphasizes evolutionary change within a species, separate from speciation
itself
• A biological species is essentially one population in the set of ancestordescendant populations in the evolutionary species
Department of Geological Sciences | Indiana University
(c) 2011, P. David Polly
G404 Geobiology
Two definitions of evolution
“Descent with modification”. (after Darwin, 1859)
• recognizes that descendant is a modified form of ancestor
• homologies are modified features inherited from ancestor
“Control of development by ecology”. (after Van Valen, 1974)
• recognizes that the phenotype of an organism is produced by
developmental processes that are only partly genetic
• by “ecology” refers to the ability of an organism to function in its
environment and in relation to other species with the phenotype
it possesses
Department of Geological Sciences | Indiana University
(c) 2011, P. David Polly
G404 Geobiology
Two kinds of evolutionary change
Modification of ancestral features
involves the inheritance of homologous structures with modification in their
size, shape, position, or function.
Examples: enlargement of openings between existing bones, reduction in the
size of bones, incorporation of bones of mandible into bones of middle ear,
modification of branchial arches into mandibular and hyoid arches, fusion of
metatarsal bones into a single tarsometatarsus
Origin of novel features
involves origin of a new feature that wasn’t present in ancestor.
Examples: origin of new bones in fins or limbs. increase in the number of
vertebrae or digits.
Department of Geological Sciences | Indiana University
(c) 2011, P. David Polly
G404 Geobiology
Homology and “analogy”
The bones of the forelimbs of pterosaurs,
bats, and birds are homologous, shared from
their common amniote ancestor (humerus,
radius and ulna, carpals, phalanges)
The wing structure is not homologous
because it evolved independently in the
three groups (wings are termed “analogous”,
or non-homologous)
Romanes, 1892 (reproduced in Bolker and Raff, 1996)
Department of Geological Sciences | Indiana University
(c) 2011, P. David Polly
G404 Geobiology
Formal definitions of homology
Corresponding structures in different organisms
[homology is] “the same organ in different
animals under every variety of form and
function” - Richard Owen, 1843
“a feature in two or more organisms is
homologous when it is derived from the same
(or corresponding) feature in their common
ancestor” - Ernst Mayr, 1982
Homology is a key concept for the interpretation
of fossil organisms, for phylogeny
recontstruction, and for understanding of
mechanisms of evolution
Criteria for homology include similarity of
structure and position, the documentation of
transitional forms in the fossil record, the study
of development (or ontogeny).
Zoology Research Collections, Naturhistoriska riksmuseet,
Stockholm (photo by P. David Polly, 2009)
Department of Geological Sciences | Indiana University
(c) 2011, P. David Polly
G404 Geobiology
Richard Owen and the vertebrate archetype
Owen (1804-1892) was the pre-eminent
paleontologist and anatomist in London
Contemporary of Queen Victoria, Charles
Darwin, and Thomas Huxley
Described many fossils, including the first
Archaeopteryx and the fossils Darwin
collected in South America
Interested in reconciling the apparent
contradictions between functional
adaptation and the structural continuity
represented by homology
Developed the idea of the vertebrate
archetype, a common structural plan from
which all vertebrates are derived
Owen, R. 1847. On the archetype and
homologies of the vertebrate skeleton. London.
Department of Geological Sciences | Indiana University
(c) 2011, P. David Polly
G404 Geobiology
Types of homology
Homology - the same structure in different organisms under every variety of
form and function inherited from the common ancestor of those organisms.
Serial homology - repetition of the same structure within an organism, such as
vertebrae, ribs, legs in arthropods, gills in fish, etc.
Deep homology - similar structures derived from the same underlying patterns
of gene expression, even if the structures have different evolutionary origins
and losses.
Primary homology - a homology recognized based on structural similarity, but
whose inheritance from a common ancestor has not been tested by
phylogenetic analysis.
Secondary homology - a homology whose evolution from a common ancestor
has been confirmed by phylogenetic analysis.
Department of Geological Sciences | Indiana University
(c) 2011, P. David Polly
G404 Geobiology
Example 1: tetrapod limb
Transformation of early tetrapod limb
involves modification of bones, loss of some
bones, addition of other bones
Sauripterus
finned tetrapod
Barameda
finned tetrapod
Tiktaalik
finned tetrapod
Formation and growth of these bones is
regulated by gene expression during
development. Changes in the regulation
result in evolutionary changes in the adult.
In earliest development, the precursors of
the bones are similar in tetrapods and their
closest relatives.
Eusthenopteron
finned tetrapod
Gogonasus
finned tetrapod
Sterropterygion
finned tetrapod
Rhizodopsis
finned tetrapod
Developmental biology (ontogeny) is an
important aid to paleontologists for
identifying or confirming homologies in
radically transformed groups
Acanthostega
limbed tetrapod
Tulerpeton
limbed tetrapod
Greererpeton
limbed tetrapod
Westlothiana
limbed tetrapod
Coates, M. I., M. Ruta, and M. Friedman. 2008. Ever since Owen: changing perspectives on the early
evolutio of tetrapods. Annual Review of Ecology, Evolution, and Systematics, 39: 571-592.
Department of Geological Sciences | Indiana University
(c) 2011, P. David Polly
G404 Geobiology
Example 2: HOX genes and regionalization
HOX (homeobox) genes control the
boundaries of morphological regions
They are shared by all bilateral
organisms, maybe all animals in
general
HOX genes are expressed in different
areas of the developing embryo in the
same order as they are found on
chromosomes
Expression of these genes create
boundaries inside which structures
develop differently, such as cervical
versus thoracic regions
Expression in
Fly Embryo
Position on
Chromosomes
Expression in
Mammal Embryo
Department of Geological Sciences | Indiana University
(c) 2011, P. David Polly
G404 Geobiology
Mutation in HOX gene doubles the axis bone (C2)
Wellik, 2009. Current Topics in Developmental Biology, 88:
257-278.
Department of Geological Sciences | Indiana University
(c) 2011, P. David Polly
G404 Geobiology
Evolution of cervical-dorsal
boundary in amniotes
Evidence for shifts in HOX expression
Müller et al., 2010. PNAS, 107: 2118-2123.
Department of Geological Sciences | Indiana University
(c) 2011, P. David Polly
G404 Geobiology
Example 3: vertebral evolution
Developing thoracic vertebra and rib in a dog
Blue = cartilage
Red = bone ossification center
Evans, 1993. Miller’s Anatomy of the Dog
Department of Geological Sciences | Indiana University
(c) 2011, P. David Polly
G404 Geobiology
Early vertebral development
Vertebrae are modeled around notochord from
somite tissue
Neural
tube
Heart
9 day mouse
embryo, before
skeletal
development
begins
Each vertebra develops between somites,
Somites
receiving tissue from one in front and one behind
Directly related to evolutionary transformations in
vertebrae of early tetrapods
Early development of the centrum in the chick (from
Patten, 1958. Foundations of Embryology.)
Department of Geological Sciences | Indiana University
(c) 2011, P. David Polly
G404 Geobiology
Anterior
Vertebral evolution in early tetrapods
Lissamphibians retain intercentrum,
amniotes retain pleurocentrum
Mastodontosaurus
Neural arch
Amniote
Intercentrum
Eryops
Pleurocentrum
Seymouria
Icthyostega
Department of Geological Sciences | Indiana University
(tree from Coates, et al. 2008. Annual Review of
Ecology, Evolution, and Systematics, 39: 571-592)
(c) 2011, P. David Polly
G404 Geobiology
Scientific papers for further reading
Bolker, J. A. and R. A. Raff. 1996. Developmental genetics and traditional homology.
Bioessays, 18: 489-494.
Coates, M. I., M. Ruta, and M. Friedman. 2008. Ever since Owen: changing perspectives on
the early evolution of tetrapods. Annual Review of Ecology, Evolution, and Systematics, 39:
571-592.
Müller, J., T. M. Scheyer, J. J. Head, P. M. Barrett, I. Werneburg, P. G. P. Ericson, D. Pol, and M.
R. Sánchez-Villagra. 2010. Homeotic effects, somitogenesis and the evolution of vertebral
numbers in recent and fossil amniotes. PNAS, 107: 2118-2123.
Polly, P. D. 2007. Limbs in mammalian evolution. Pp. 245-268, in Fins into Limbs: Evolution,
Development, and Transformation, Brian K Hall (ed.). University of Chicago Press: Chicago.
Wellick, D. M. 2009. Hox genes and vertebrate axial pattern. Current Topics in
Developmental Biology, 88: 257- 278.
Department of Geological Sciences | Indiana University
(c) 2011, P. David Polly