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1 Review article – A system for analysing features
2 in studies integrating ecology, development, and
3 evolution
4 J. R. STONE1,2,* and B. K. HALL1,*
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Biology Department, Dalhousie University, Life Sciences Building, 1355 Oxford Street, Halifax NS
B3H 4J1, Canada; 2Department of Biology, McMaster University, Life Sciences Building, 1280 Main
Street West, Hamilton ON, Canada L8S 4K1; *Author for correspondence(e-mail: jstoner@
mcmaster.ca and [email protected]; phone: +905-525-9140; fax: +905-522-6066)
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Received 24 September 2003; accepted in revised form 4 March 2005
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10 Key words: Adaptation, Homology, Morphology, Ontogeny, Phylogeny
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Abstract. Ecology is being introduced to Evolutionary Developmental Biology to enhance
organism-, population-, species-, and higher-taxon-level studies. This exciting, bourgeoning troika
will revolutionise how investigators consider relationships among environment, ontogeny, and
phylogeny. Features are studied (and even defined) differently in ecology, development, and
evolution. Form is central to development and evolution but peripheral to ecology. Congruence
(i.e., homology) is applied at different hierarchical levels in the three disciplines. Function is
central to ecology but peripheral to development. Herein, the supercategories form (‘isomorphic’
or ‘allomorphic’), congruence (‘homologous’ or ‘homoplastic’), and function (‘adaptive’ or
‘nonadaptive’) are combined with two developmental mode (i.e., growth) categories (‘conformational’ or ‘nonconformational’) to provide a 16-class system for analysing features in studies in
which ecology, development, and evolution are integrated.
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Now that developmental and evolutionary biology are reacquainted and united
as ‘Evolutionary Developmental Biology’ (Gould 1977; Raff 1996; Larsen et al.
1997; Hall 1999), biologists have begun to introduce a previously uninvited
guest, ecology, to the affair (Schlichting and Pigliucci 1998; Hall 1999; Gilbert
2001). Currently, too few biological systems are understood comprehensively
from ecological, developmental, and evolutionary perspectives to achieve the
ménage à trois, although ecology and evolution have been flirting for a long
time in adaptation, behavioural ecology, life history, and phenotypic plasticity
studies. Nevertheless, integrating ecology would benefit biologists because,
then, phylogeny could be considered more-completely as modification over
time that is wrought by environmental effects on ontogeny (van Valen 1973;
Matsuda 1987; Gerhart and Kirschner 1997; Schlichting and Pigliucci 1998;
Hall 1999, 2001; Hall et al. 2003). In this paper, three binary ‘supercategories’
are coupled with two developmental mode categories to provide a 16-class
system for analysing features in studies that integrate ecology, development,
and evolution. The supercategories constitute form, congruence, and function.
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AUTHOR’S PROOF!
Springer 2005
Biology and Philosophy (2005) 00:1–15
DOI 10.1007/s10539-005-3181-3
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The developmental mode categories comprise ‘conformational’ or ‘nonconformational.’
The coupling is achieved by considering ‘traits’ as real (a posteriori-perceived) manifestations that result from interactions at ecological, developmental, and evolutionary levels and ‘features’ as ideal (a priori-apprehended)
intuitions that biologists may use to synthesise conceptually perspectives from
these levels. Definitions for these terms are presented in the section ‘Traits and
features.’ Those definitions are used to describe the supercategories in the
sections ‘Form: isomorphic and allomorphic features;’ ‘Congruence: homologous and homoplastic features;’ ‘Function: similar and dissimilar environment
features;’ and ‘Growth: conformational and nonconformational features;’
therein, definitions, descriptions, and examples are provided to elucidate the
categories ‘isomorphic’ or ‘allomorphic;’ ‘homologous’ or ‘homoplastic;’
‘adaptive’ or ‘nonadaptive;’ and conformational or nonconformational. These
categories are utilised to develop a ‘hexakaidecagonal’ system for classifying
features, which is expounded in the antepenultimate section, ‘A 16-class system
for analysing features,’ and exemplified in the penultimate section, ‘Exemplifying the 16-class system.’ A brief synopsis is presented in the final section,
‘Prospectus.’
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Synthesising ecology with developmental and evolutionary biology will require
introducing many new technical terms or redefining old ones. Some technical
terms – homology, for instance – have long histories. Utilising them in a new
context – homology as percent similarity, for instance – is undesirable, although homology has been applied legitimately to newly discovered biological
hierarchy levels, such as homologous as genes, gene networks, or developmental processes (Wagner 1989; Hall 1994, 1995; Abouheif 1997; Gilbert and
Bolker 2001; Wilkins, 2002).
Terminology that is associated with organism characteristics obviously is
important and should be precise but, also, intuitive. After all, a part is a part, is
a part. However, neither terminology nor related assumptions, concepts, or
theories that are associated with parts have been agreed upon universally
(Riedl 1978; Gans 1988; Wake 1992).
Herein, traits are defined as observable properties that are exhibited by
individuals at any level, from microscopic to macroscopic (e.g., ‘collagen
type in specimen 17, as determined by transmission electron microscopy’ or
‘vertebral number in specimen 42, as determined by X-radiography’). Features are considered as categorical sets to which all the variation that is
exhibited by corresponding traits within taxa can be assigned (e.g.,
‘echinoderm mutable collagen’ or ‘vertebrate trunk’); this consideration for
features is a refinement with respect to the definition that was provided by
Bock and von Wahlert (1965, p. 271), who were interested in associating
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59 Traits and features
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form and function in identifying adaptive features: ‘‘[a]ny part … of an
organism will be referred to as a feature if it stands as a subject in a
sentence descriptive of that organism’’ (additional discussions concerning
features are contained in (Riedl 1978 – especially pp. 89–92, Gans 1988;
Wake 1990, 1992).
Features may be ascribed to 16 classes that are defined on the basis of the
binary supercategories form, congruence, function, and growth (i.e., 24 = 16).
The categorical combinations that constitute those classes comprise a (possibly
non-nested) biological hierarchy (Hall 1994) that can be utilised for feature
systematisation (Table 1 nAu: Table 1 is cited but not supplied. Please
check.n). Using this system to analyse features will entice evolutionary developmental biologists to integrate ecology into their research programmes and
philosophies and, thereby, facilitate the aforementioned conceptual synthesis
among ecology, development, and evolution.
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96 Form: isomorphic and allomorphic features
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Feature form may be described using size or shape, among other variables
(e.g., position or topology). Size can be measured unambiguously, qualitatively
(e.g., ‘elongated’) and quantitatively (e.g., ‘comprising 14 vertebrae’). Shape
can be measured unambiguously only by implementing biometric statistic
techniques, such as multivariate statistics (e.g., Reyment et al. 1984) or geometric morphometrics (e.g., Rohlf and Marcus 1993). Implementing biometric
statistic techniques yields a more-precise definition than that was provided by
Bock and von Wahlert (1965, pp. 272–273): ‘‘In any sentence describing a
feature of an organism, its form would be the class of predicates of material
composition and the arrangement, shape or appearance of these materials,
provided that these predicates do not mention any reference to the normal
environment of the organism.’’ Isomorphic features exhibit similar shapes or
structures; allomorphic features exhibit dissimilar shapes or structures.
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[f]orm is both deeply material and highly spiritual. It cannot exist without
a material support; it cannot be properly expressed without invoking
some supra-material principle. Form poses a problem which appeals to
the utmost resources of our intelligence, and it affords the means which
charm our sensibility and even entice us to the verge of frenzy. (Dalcq
1968, p. 91).
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117 Congruence: homologous and homoplastic features
118 The terms ‘homology’ and ‘homoplasy’ may be defined on the basis of
119 many criteria (Hall 1994, 1995, 2003a, b; Bock and Cardew 1999).
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Consequently, precise unanimously accepted definitions are wanting. Owen
(1843, p. 379, 374) defined a ‘homologue’ as the ‘‘same organ in different
animals under every variation of form and function’’ and its antithesis, an
‘analogue,’ as a ‘‘part of organ in one animal which has the same function
as another part or organ in a different animal.’’ These definitions were
published prior to Darwin’s (1859) magnum opus and, so, lacked an evolutionary perspective.
Worried that Owen’s term homology was rife with Platonic idealism and
prone to misconstruction in typological and archetypical terms, Lankester
(1870, p. 36) introduced two terms to distinguish two similarity (i.e., homology)
classes: ‘homogeny’ for features that were similar from immediate shared
ancestry; and ‘homoplasy’ for features that were similar from independent
evolution (Hall 2003b). That introduction might have constituted the first instance wherein homology was conceptualised within an evolutionary context.
Ironically, the term homogeny has become extinct from evolutionary terminology, whereas the term homoplasy has been redeployed antithetically to
homology Brooks and McLennan 1991; Hall 1994, 1999, 2001, 2002, 2003b;
Sanderson and Hufford 1996; Wake 1996, 1999; Meyer 1999).
Contemporary homology and homoplasy descriptions involve a variety of
technical terms that are associated with cladistic analysis, including ‘character
statements,’ ‘character states,’ ‘outgroups,’ ‘ingroups,’ ‘plesiomorphic,’ ‘apomorphic,’ and ‘synapomorphic.’ In parsimony based cladistic analyses,
hypotheses concerning features are formalised using character statements (e.g.,
‘trunk form’). The character states into which character statements are encoded
represent the physical manifestations that are subjected to hypothesis testing
(e.g., ‘normal’ or ‘elongate’).
Character states are defined on the basis of comparative analyses between (at
least two) taxa comprising a reference group, the ‘outgroup,’ and taxa in a
study group, the ‘ingroup.’ Character states are classified as either shared
among outgroup and ingroup taxa (‘plesiomorphic character states’) or unique
to ingroup taxa (‘apomorphic character states’). Clades are taxon sets that are
classified on the basis of shared apomorphic (‘synapomorphic’) character
states. Each synapomorpic character state may be considered as a particular
information bit (i.e., a binary decision) that was obtained from a comparative
analysis involving a feature, an unfalsified clade-membership hypothesis. A
cladogram may be considered as that clade arrangement that minimises falsified clade-membership hypotheses (more-detailed definitions are provided in
Brooks and McLennan 1991).
On the basis of the foregoing prescriptions, feature congruence may be defined operationally: homologous features are those that can be represented on
a cladogram by unique synapomorphic character states (i.e., solitary unfalsified
clade-membership hypotheses); homoplastic features are those that cannot be
so represented (i.e., multiply falsified clade-membership hypotheses).
Patterson (1982) and Larson and Losos (1996) described three criteria that
may be applied to test putative homologous features:
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165 • the ‘similarity criterion’ – topographic, ontogenetic, and compositional cor166 respondence – concerns comparable feature form, development, and position;
167 • the ‘congruence criterion’ – the homologous feature criterion that is en168 dorsed herein – involves deducing whether features may be represented as
169 synapomorphic character states; and
170 • the ‘conjunction criterion’ – homologous features cannot coexist in indi171 vidual organisms – entails that putative homologous features within indi172 vidual organisms are mutually excluding (i.e., it prohibits inappropriate
173 comparisons among ‘serial homologous features,’ which are produced by
174 duplication and divergence).
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Elongated trunks among bolitoglossine salamanders fail to satisfy the sim176 ilarity criterion because trunk elongation is achieved by increasing individual
177 vertebrae length in members of the genus Lineatriton but by increasing verte178 brae number in members of the genera Oedipina and Batrachoseps and some
179 members in Lineatriton (Wake 1966; Parra-Olea and Wake 2001).
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Bird and bat wings fail to satisfy the congruence criterion because they
181 cannot be represented as a unique synapomorphy on a cladogram (i.e., on the
182 basis of exclusion according to synapomorphic character states that are de183 duced from other vertebrate features; Coddington 1988; Larson and Losos
184 1996).
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Fly halteres and other insect hindwings satisfy the conjunction criterion
186 because homeotic Bithorax mutant flies possess four wings but no halteres [i.e.,
187 they are homologous as flight appendages; Waddington (1956); a gene regu188 lation perspective for their disjunction is presented in Gibson (1999)].
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These three criteria may be utilised to define precisely two homoplastic
190 feature types. Those that fail to satisfy only the congruence criterion result
191 from parallel evolution and are known as ‘parallel features.’ Those that fail to
192 satisfy the similarity and congruence criteria result from convergent evolution
193 and are known as ‘convergent features.’ Parallel features originate multiple
194 times via similar developmental processes from similar ancestral conditions
195 and often constitute the data in developmental constraint hypothesis tests (e.g.,
196 Wake 1991; Larson and Losos 1996; instances are provided in Hall 2002,
197 2003a, b). Convergent features originate independently, bear superficial
198 resemblances, and often constitute the data in adaptation hypothesis tests
199 (Brooks and McLennan 1991; Coddington 1994).
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The distinction between parallel and convergent evolution, or ‘parallelism’
201 and ‘convergence,’ can be elucidated unambiguously with molecular genetic
202 data. Parallelism may be defined as change to a particular character state (e.g.,
203 nucleotide base or amino acid codon) from the same character state indepen204 dently in multiple groups (e.g., adenine A to cytosine C in two groups);
205 whereas convergence entails change to a particular character state from dif206 ferent character states (e.g., A to C from guanine G in one group and from
207 thymidine T in another).
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Gans (1985) used Venn diagrams to allot current (masticatory) feature
209 similarities to three different sets. Structure sets contain elements exhibiting
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similar appearances, shapes, topographical relations, vascularisations, innervations, and material compositions. Development sets contain elements
exhibiting similar temporal and mechanistic ontogenies, embryologies, and
genetic bases. Function sets contain elements exhibiting similar mechanisms
and physical and chemical activities. Gans identified homoplastic features that
served the same function (analogues) as useful for characterising functional
constraints.
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217 Function: similar and dissimilar environment features
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Nonadaptive features are those for which there were no feature-environment
associations upon origin. Derivative terms for these features include: ‘exaptations’ – features with current utilities that differ from those that were associated
with their origin (Gould and Vrba 1982), ‘nonaptations’ – features that confer
no advantages to organisms possessing them (Gould and Vrba 1982), and
‘disaptations’ – features that confer a disadvantage to organisms possessing
them (Larson and Losos 1996).
Brooks and McLennan (1991) presented a scheme for assigning putative
adaptations to one among eight categories. The scheme was derived craftily, by
synthesising environmental criteria with traditional character classification
categories and, simultaneously, integrating that synthesis with an independent
congruence assignment. Thereby, the four traditional character classification
categories – similar features among related taxa (homologous features); similar
features among unrelated taxa (convergent features); dissimilar features among
related taxa (divergent features); and dissimilar features among dissimilar taxa
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218 Although function cannot be utilised legitimately to categorise features as
219 homologous or homoplastic (Gilbert and Bolker 2001), the association be220 tween function and environment can provide information that is useful for
221 inferring developmental modes and, thereby, categorisation. Feature function
222 may be described in accordance with the term ‘aptive,’ which refers to the
223 advantages that are conferred to organisms possessing particular features –
224 literally, ‘fitting’ them for particular conditions (Darwin 1859; Gould and Vrba
225 1982). Furthermore, adaptive features exhibited direct associations with the
226 environments in which those features originated – signified by the prefix ‘ad,’
227 thus, literally ‘toward’ those conditions (Gould and Vrba 1982; Baum and
228 Larson 1991; Larson and Losos 1996). This dissociation between function and
229 environment is similar to the definition that was provided by Bock and von
230 Wahlert (1965, p. 273):
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232 In any sentence describing a feature of an organism, its functions would
233 be that class of predicates which include all physical and chemical
234 properties arising from its form … including all properties arising from
235 increasing levels of organisation, provided that these predicates do not
236 mention any reference to the environment of the organism.
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252 (nonhomologous features) – were refined and each decomposed into two. This
253 increased resolution enables decoupling pattern and process:
254 • isomorphic features that persist in similar environments may be inferred to
255 be effected by selection if the traits are homologous but may be inferred to
256 represent adaptive parallelism or convergence if they are homoplastic;
257 • isomorphic features that persist in dissimilar environments may be inter258 preted as being retained as a consequence of phylogenetic constraint if the
259 traits are homologous but may be interpreted as being retained as a conse260 quence of nonadaptive parallelism or convergence if they are homoplastic;
261 • allomorphic features that persist in similar environments may be considered
262 as products from divergence if the traits are homologous but may be con263 sidered distinct if the traits are homoplastic;
264 • allomorphic features that persist in dissimilar environments may be posited
265 as resulting from adaptive divergence if they are homologous but may be
266 posited as different if homoplastic.
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The similarity criterion that was proposed by Patterson (1982) involves shared
development; thus, it may be considered as a successor to (Lankester’s 1870)
two homology classes, (Balfour’s 1880) ‘complete’ and ‘general’ homology, and
(Wilson’s 1891) ‘‘complete’’ and ‘‘incomplete’’ homology notions (Hall 1999,
2000, 2003a, b). Conformational features are defined herein as those that exhibit comparable development, whereas nonconformational features are those
for which development is noncomparable. This dichotomy is less discrete than
are those that are associated with congruence (homologous or homoplastic
features) or function (adaptive or nonadaptive features), which can be defined
operationally according to cladistic terminology. Furthermore, unlike the case
with form (wherein the designations isomorphic and allomorphic are amenable
to biometric statistic techniques), currently, there is no metric for gauging
comparability for development. Therefore, categorisation as conformational
and nonconformational involves less precision and more continuity but, when
combined with the other categorisations (i.e., those that are determined on the
basis of form, congruence, and function), can provide a means for analysing
features.
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267 Growth: conformational and nonconformational features
285 A 16-class system for analysing features
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Among ecology, development, and evolution, the criteria that were endorsed
by Patterson (1982) for homology and by Larson and Losos (1996) for
adaptation involve development (similarity) and evolution (congruence); the
sets that were defined by Gans (1985) for similarity involve development
(development sets) and ecology (function sets); and the scheme that was presented by Brooks and McLennan (1991) for adaptation involves evolution (i.e.,
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292 homoplastic or homologous) and ecology (i.e., nonadaptive or adaptive). By
293 synthesising these prescriptions with the two developmental mode (i.e., growth)
294 categories (conformational and nonconformational), a 16-class system for
295 analysing features that are involved in ecological-developmental-evolutionary
296 hypotheses can be established (Table 1). In particular,
297 • features may be assessed as isomorphic or allomorphic;
298 • character states representing those features can be optimised on cladograms
299 to classify them as homoplastic or homologous;
300 • environments in which specific taxa possessing those features reside can be
301 considered to assign them as either adaptive or nonadaptive; and finally,
302 • developmental modes can be considered or those developmental modes that are
303 consistent with particular pattern combinations (i.e., isomorphic or allomor304 phic, homoplastic or homologous, and similar or dissimilar environment) may
305 be inferred to designate features as conformational or nonconformational.
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Developmental mode inferences may be transformed into hypotheses that
307 subsequently can be subjected to the similarity criterion (Patterson 1982) for
308 testing.
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Constructional morphologists, whether neontologists or palaeontologists,
310 have prescribed syntheses that are similar to the one that is presented herein,
311 invoking ecological adaptation, ‘architecture or construction laws’ (develop312 mental mechanisms, engineering principles, geometric rules, or material
313 properties), biomechanics, and phylogeny in their analyses (e.g., Rudwick
314 1964; Raup 1966, 1972; Seilacher 1970; Dullemeijer 1974; Raup and Stanley
315 1978; Stanley 1979; Hickman 1980; Reif et al. 1985; Hall 2002). The advantage
316 that is conferred by the 16-class system derives from the means with which
317 information from a variety of sources is combined and synthesised. For in318 stance, because ontogenies for nonadaptive features are autonomous from
319 environmental influences, if a nonadaptive feature were to appear multiple
320 times in a group, then comparable developmental modes could be inferred.
321 Exemplifying the 16-class system
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322 The 16-class system can be used to classify biological phenomena on the basis
323 of patterns (Table 1; instances for each ensue).
324 Selection: isomorphic, homologous, similar environment
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Brooks and McLennan (1991) proposed that isomorphic homologous features
that are observed in similar environments could be inferred to have been
produced by stabilising selection. They conceded that such inferences constitute weak explanations for failed adaptation tests, because no comparisons
involving function-with-environment-change can be performed; indeed, from
the Bumpus (1898) sparrows to the Kettlewell (1955) moths, empirical data
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that have been purported to instantiate stabilising selection have been controversial. Nevertheless, a conformational selectively stable feature is epitomised by the human appendix; given its uncertain function, its retention cannot
be considered adaptive, despite controversy. Other selection modes are possible. For instance, in a remarkable case instantiating directional selection
involving nonconformational features, Rutledge et al. (1974) observed that,
after seven generations, several members in inbred mice lines possessed equally
elongated tails. Similar to the situation in bolitoglossine salamanders (discussed previously and subsequently), some members in those inbred-lines
achieved elongation with fewer and longer vertebrae than occurred in members
in unselected lines, whereas others achieved elongation with additional but
shorter vertebrae. In contrast to Patterson (1982), herein, as in Hall (1995),
these features are considered to be homologous as elongated tails.
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344 Phylogenetic constraint: isomorphic, homologous, dissimilar environment
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Phylogenetically constrained conformational features are evolutionary novelties, such as chordate notochords. The seemingly paradoxical case involving a
phylogenetically constrained nonconformational feature is elucidated ironically with that feature that caused Darwin (1859) the greatest concern. In most
vertebrates, eye lenses form via ectoderm induction (the final step in an
induction cascade) by the optic vesicle (Grainger 1992; Grainger et al. 1998
nAu: The year 1988 in Grainger et al. is changed to 1998 to match with the list.
Please checkn; Hall 1999). However, eye development is variable in urodele
and anuran species. For instance, whereas eye lenses form in the typical vertebrate manner in the frog species Rana fusca, eye lenses form with no
induction from the optic cup in the congeneric species R. exculenta (de Beer
1971; Jacobson and Sater 1988; Hall 1999). Development evolves!
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357 Adaptation: isomorphic, homoplastic, similar environment
Adaptive parallelism may be demonstrated with molecular data, whenever
function can be correlated with molecular modifications yielding conformational features. For instance, lysozyme is an enzyme that is involved in bacterial resistance in many vertebrate cells or tissues (e.g., macrophages, tears,
saliva, avian egg-white, mammalian milk). Sequence analysis revealed that
particular amino acids that are present in some foregut-fermenting vertebrates
(i.e., ruminants, colobine monkeys, hoatzins) most-likely were produced by
mutations that altered the same initial amino acids and, thereby, constitute
adaptive parallel features (Zhang and Kumar 1997). Nonconformational features that exhibit pattern combinations that characterise adaptive convergence
are exemplified by classic analogy. Fish fins and cetacean flippers or
insect, bird, and bat wings function similarly but are produced by different
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370 developmental modes (Hall 1995, 1999, 2005); similarly, the spines on New
371 World Cactaceae, which are modified leaves, resemble the thorns on Old
372 World Euphorbiaceae, which are modified branches (Niklas 1997).
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Brooks and McLennan (1991) suspected that nonadaptive convergence comprised pattern combinations that were ‘‘driven’’ by development. According to
the categorisation system that is presented herein, these features must be conformational. For instance, they could result from channelling constraints (sensu
Gould 1989; i.e., constraints wherein a feature is produced by one among many
discrete possible ontogenetic trajectories). These feature types accord to
(Darwin’s 1859) ‘‘rules of growth,’’ for which Gould (1989) cited shells that
characterise the Caribbean land snail genus Cerion as prime instances. Shells that
typify this genus exhibit covariance in many characteristics and may be grouped
generally into two morphotypes: the ribby morphotype is characterised by a
thick shell with a triangular apex and few coarse ribs; the mottled morphotype is
characterised by a thin shell with a barrel-shaped outline and numerous fine ribs
(or none at all). Ribby forms are restricted to bank-edge coasts, whereas mottled
forms are restricted to bank-interior coasts and island interiors (Gould and
Woodruff 1986). If features were nonconformational, then the pattern combination isomorphic, homoplastic, dissimilar environment could result from
nonadaptive parallelism. For instance, a cladistic analysis involving mitochondrial DNA data revealed that the bolitoglossine salamander genus Lineatriton is
polyphyletic: individuals in L. lineolus (the lone species) from different localities
comprised members in two distinct clades in which L. lineolus comprised a sister
group to difference species in the genus Pseudoeurycea (Parra-Olea and Wake
2001). Therefore, vertebral length increase, as one among at least two possible
environmentally autonomous developmental modes by which trunk elongation
can be achieved, has occurred twice during bolitoglossine salamander evolution,
and each occurrence constitutes a parallel feature.
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373 Nonadaptation: isomorphic, homoplastic, dissimilar environment
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399 Nonadaptive divergence: allomorphic, homologous, similar environment
Brooks and McLennan (1991) claimed that nonadaptive divergence comprised
pattern combinations that were ‘‘allowed’’ by development during vicariant
biogeographic events and allopatric speciation. According to the system that is
presented herein, this situation could arise only if a feature is conformational. In
this case, the feature could be produced by a labile ontogenetic trajectory –
developmental flexibility – and may be considered as the nonadaptive counterpart to phenotypic plasticity or adaptively neutral genetic assimilation (Hall
1999, 2001, 2003c). For instance, six different aortic arch patterns are observed in
rabbits, even though variability is accounted for predominantly by two
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11
(Edmonds and Sawin 1936; Sawin and Edmonds 1949). If the feature were
nonconformational, then it could exemplify adaptive convergence. For instance,
crustacean mouthparts are derived evolutionarily from paired limbs – homeotic
mutation, and this homology hypothesis is supported by Hox, Ubx, and AbdA
gene expression suppression in anterior trunk segments (Averof and Patel 1997).
OF
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410
411
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414 Adaptive divergence: allomorphic, homologous, dissimilar environment
ED
PRO
Adaptive divergence could occur if environmental change effected (i.e., brought
about) morphological change without concomitant developmental change.
This phenomenon is known as phenotypic plasticity (Schlichting and Pigliucci
1998). For instance, eyespot size on wings for the African satyrine butterfly
Bicyclus anynana is increased with temperature increases, a response that
confers increased fitness during the warm, wet season by providing enhanced
predator avoidance via false-eye mimicry (Brakefield et al. 1996; Brakefield
1997). Adaptive divergence also could occur if development were altered via
genomic evolution. For instance, species in the daisy tree genus Montanoa
present diploid shrub forms in relatively xeric lowland areas and polyploid tree
forms in relatively moist cloud forests at higher elevations (Funk 1982; Brooks
and McLennan 1991); the shrub forms are nonviable in moist conditions,
whereas the tree forms are nonviable in xeric conditions.
ECT
415
416
417
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419
420
421
422
423
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425
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427
428 Different: allomorphic, homoplastic, similar environment
ORR
The classic interpretation that invertebrate and vertebrate eyes are analogous
as visual organs exemplifies features that are different. Interestingly, depending
on the analysis type and level, this instance can be interpreted to satisfy nonconformational and conformational cases, as there is remarkable gene conservation involved in eye development regulation. For instance, on the basis of
sequence similarity, intron splice position conservation, expression identity,
and mutational effects, the genes eyeless (in arthropods) and Pax-6 (in vertebrates) are hypothesised to be orthologous (i.e., homologous as DNA sequences). If developmental modes were considered as occupying the same
hierarchical levels that are occupied by genes, then eyes would be different
conformational features; however, if developmental modes were considered as
occupying different hierarchical levels than those that are occupied by genes,
then eyes would be different nonconformational features.
UNC
429
430
431
432
433
434
435
436
437
438
439
440
441
442 Distinct: allomorphic, homoplastic, dissimilar environment
443 Distinct features differ in form, congruence, and function. Conformational
444 distinct features share a common developmental mode. For instance,
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belly-ectoderm-to-prospective-face-region transplants between neurula-stage
frog and newt embryos produce newt larvae with no balancer organs and newtectoderm-derived cement glands comprising neural crest cells; and frog larvae
with frog-odontoblast-derived dentine teeth that include newt enamel and
balancers (ordinarily, newts possess balancer organs, which are epithelial tubes
that are stiffened internally by neural-crest-derived connective tissue, and no
cement glands, whereas frog larvae possess no dentine teeth and no balancers).
These remarkable results demonstrate comparable tissue inductions, even
spatially (differences between frog and newt faces are attributable to differences
in ectoderm responses; Gerhart and Kirschner 1997). Distinct features also can
be produced by noncomparable developmental modes; relations between these
features are superficial and meaningful only as an exercise in the etymology
that is used to associate them. For instance, proboscis among invertebrates
(e.g., echiuran probosci) and vertebrates (e.g., elephant trunks) are distinct.
PRO
445
446
447
448
449
450
451
452
453
454
455
456
457
458
ORR
ECT
Features constitute appropriate constructs for establishing research programmes in ecology-developmental-evolutionary biology, because they abstract from trait sets those properties that derive from interactions at multiple
(i.e., ecological, developmental, and evolutionary) levels. Using the 16-class
system, eco-devo-evo biologists can utilise patterns to integrate ecological,
developmental, and evolutionary information. Researchers can use data that
may be obtained by perusing literature to determine supercategory-developmental mode combinations for any feature and, thereby, classify it. This pluralistic approach affords more-thorough comprehension concerning how
features are affected by environments, effected in development, and transformed during evolution than do more-conventional approaches. This approach also enables finer resolution in inference when some information is
lacking; to reiterate an example, a nonadaptive feature that appears multiple
times in a group may be inferred to have been derived from comparable
developmental modes, and, therefore, the multiple occurrences constitute
parallelisms. Thereby, the hexakaidecagonal system couples pattern (e.g., a
nonadaptive feature that appears multiple times in a group) and process (e.g.,
parallel evolution) in feature studies.
UNC
460
461
462
463
464
465
466
467
468
469
470
471
472
473
474
475
476
477
ED
459 Prospectus
478 Acknowledgements
479
480
481
482
483
Comments and inspiration during manuscript development and evolution were
provided by A. Cameron, A. Cole, M. Connolly, K. Downing, M. Dymond,
T. Fedak, H.-T. Kim, H. Knoll, D. Krailo, W. Olson, T. Thornhill,
M. Vickaryous, N. Vincent, an anonymous referee, and K. Sterelny. Funding
that provided the working environment for this work was provided by the
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484 Canadian Institutes of Health Research (JRS), Killam Trust of Dalhousie
485 University (BKH), and Natural Sciences and Engineering Research Council of
486 Canada (Grants 261590 to J.R.S. and A5056 to B.K.H.).
487 References
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