Defining sameness: historical,
biological, and generative homology
Ann B. Butler
1
* and William M. Saidel
2
Summary
Current debate concerning homology arises from three
different research interestsÐphylogenetics, character
evolution, and generative pathways. Phylogenetic
homology focuses on descent of the character from a
common ancestor. Biological homology addresses
character evolution and diversification. Exceptions to
the general case complicate these two approaches:
historically and biologically homologous characters
may be produced by different generative pathways,
and minutely similar characters produced by the same
generative pathways may have a sporadic phylogenetic
distribution. We suggest that for studies of comparative
developmental biology, new descriptive terms are
needed to distinguish similar structures that result from
the same generative pathways from those that result
from different generative pathways. The terms syngeny,
meaning ``same genesis'', and allogeny, meaning ``dif-
ferent genesis'', allow the acknowledgement of same-
ness at the generative level and can be used in
combination with the terminology of historical homol-
ogy and biological homology to describe any given
character. BioEssays 22:846±853, 2000.
ß 2000 John Wiley & Sons, Inc.
Introduction
The field of comparative biology is unified in its interest in
evolutionary patterns and processes, and the concept of
homology is central to it.
(1)
Homology was defined by Owen
in 1843 as ``the same organ in different animals under every
variety of form and function'',
(2)
but the meaning of the word
``same'' still remains to be agreed upon.
(3)
The concept of
homology has remained elusive,
(4)
due in part to the different
and not always overlapping aspects of sameness that
comparative biological studies address (Ref. 5 and G.P
Wagner, pers. comm). Morphogenesis, structural similarity,
and phylogeny do not always coincide: sameness as defined
by the same genetic and/or developmental bases for a
character is not in all instances consistent with sameness at
the phenotypic level or with sameness as defined by a
monophyletic distribution of a shared derived character.
(6±8)
Recent studies on the genetic and developmental bases
for adult phenotypic structures have revealed that the degree
of generative sameness across diverse taxa is considerably
more extensive than previously appreciated. Homology of
characters has been inferred from shared generative path-
ways. New insights and research programmes sometimes
require new terminology in order to express findings
concisely and without ambiguity. We propose here that
new terms are needed to clarify character relationships for
studies in comparative developmental biology: syngeny,or
generative homology, and allogeny,orgenerative homo-
plasy, to characterize the relationship of a given character
across taxa that is produced either by shared generative
pathways or by different generative pathways, respectively.
G.P. Wagner (pers. comm.) recognizes three different
research interests that address different aspects of same-
ness and comparative biology. The first of these interests is
phylogenetics and systematics. It is served by the concept of
phylogenetic, or historical, homology (synapomorphy) and is
concerned with the reconstruction of phylogenetic relation-
ships and the recognition of monophyletic groups. It
addresses character distribution. The second interest is
character evolution, or phenotypic evolution. It is served by
the concept biological homology, which is concerned with
character evolution and character diversification across a
phylogeny. It addresses the mechanisms of character
evolution. Biological homology invokes developmental me-
chanisms to account for variational tendencies but does not
define sameness by shared generative pathways. The third
interest is comparative developmental biology. It is served by
the new concept of generative homology, or syngeny, which
is concerned with the evolution of the generative pathways
for characters. It addresses the processes of character
development. As Wagner (pers. comm) notes, generative
homology, historical homology, and biological homology
usually overlap and imply each other, but occasionally they
can be independent.
Homology and comparative biology
Homology has been designated the ``hierarchical basis of
comparative biology''
(6,9)
in recognition of the multiple levels
846 BioEssays 22.9 BioEssays 22:846±853, ß 2000 John Wiley & Sons, Inc.
1
Krasnow Institute for Advanced Study and Department of Psychology,
George Mason University, Fairfax, Virginia.
2
Department of Biology, Rutgers University, Camden, New Jersey.
Funding agencies: NSF Grant number: IBN-9728155 to ABB, a
Whitehall Foundation grant and NSF Grant number: IBN-9723562 to
WMS, and The Krasnow Institute for Advanced Study at George
Mason University.
Correspondence to: Dr. Ann B. Butler, Krasnow Institute for Advanced
Study MSN 2A1, George Mason University, Fairfax, VA 22030. E-mail:
ABButler@gmu.edu
Problems and paradigms