EVOLUTION & DEVELOPMENT

13:2, 214 227 (2011)

DOI: 10.1111/j.1525-142X.2011.00471.x

What is parallelism?
Robert W. Scotland
Department of Plant Sciences, South Parks Road, University of Oxford, Oxford, OX1 3RB, UK
Author for correspondence (email: robert.scotland@plants.ox.ac.uk)

SUMMARY Although parallel and convergent evolution are discussed extensively in technical articles and textbooks, their meaning can be overlapping, imprecise, and contradictory. The meaning of parallel evolution in much of the evolutionary literature grapples with two separate hypotheses in relation to phenotype and genotype, but often these two hypotheses have been inferred from only one hypothesis, and a number of subsidiary but problematic criteria, in relation to the phenotype. However, examples of parallel evolution of genetic traits that underpin or are at least associated with convergent phenotypes are now emerging. Four criteria for distinguishing parallelism from convergence are reviewed. All are found to be incompatible with any single proposition of

homoplasy. Therefore, all homoplasy is equivalent to a broad view of convergence. Based on this concept, all phenotypic homoplasy can be described as convergence and all genotypic homoplasy as parallelism, which can be viewed as the equivalent concept of convergence for molecular data. Parallel changes of molecular traits may or may not be associated with convergent phenotypes but if so describe homoplasy at two biological levelsFgenotype and phenotype. Parallelism is not an alternative to convergence, but rather it entails homoplastic genetics that can be associated with and potentially explain, at the molecular level, how convergent phenotypes evolve.

INTRODUCTION
A perennial issue of unresolved discussion in biology is the distinction between parallel and convergent evolution (Scott 1891, 1896; Hennig 1966; Reidl 1979; Saether 1979; Patterson 1982, 1988; Rieppel 1988; Donoghue 1992; Sanderson and Huord 1996; Abouheif 1997, 1999; Abouheif et al. 1997; Wray and Abouheif 1998; Wichman et al. 1999; Abouheif and Wray 2002; Gould 2002; Cooper et al. 2003; Sucena et al. 2003; Cracraft 2005; Christin et al. 2007; Hall 2007; Arendt and Reznick 2008a, b; Rokas and Carroll 2008; Scotland 2010). In a recent article Arendt and Reznick (2008a) claim that parallelism is a superuous term and that convergence suces to describe all occurrences of the independent evolution of the same phenotype. Ironically, this reformulation comes at a time, when the term parallelism is enjoying something of a resurgence in interest among evolutionary biologists (Zhang and Kumar 1997; Gould 2002; Cooper et al. 2003; Sucena et al. 2003; Colosimo et al. 2005; Fong et al. 2005; Harrison et al. 2005; Derome et al. 2006; Roberge et al. 2006; Christin et al. 2007; Rokas and Carroll 2008; Liu et al. 2010). Goulds (2002, p. 1089) excitement epitomized in a triumphalist tone usually shunned in science, but clearly justied in this rare case stated that Parallelism has now, and nally after a century of terminological recog214

nition, become an operational subject for evolutionary research. Arendt and Reznick (2008a) distinguish parallelism from convergence on the basis of whether taxa that share independently acquired phenotypic traits are closely or distantly related. This contrasts with the views of others, that distinguish parallelism from convergence on the basis of whether or not the same genetic mechanisms are involved (e.g., Haas and Simpson 1946; Gould 2002; Hall 2007) whether or not they are the same trait (e.g., Patterson 1982; Patterson 1988) or whether they have the same or dierent ancestral character states (e.g., Hennig 1966; Rokas and Carroll 2008). One reason this issue is of signicance is that under some (but not all) formulations, parallelism is a term that attempts to link the phenotype with the genotype; a link that represents a central theme in contemporary developmental and evolutionary biology (Scotland 2010 and references therein). The uncertainty that surrounds parallelism and convergence often results in the same evolutionary phenomena being described as belonging to dierent categories. For example, two studies entitled C4 photosynthesis evolved in grasses via parallel adaptive genetic changes (Christin et al. 2007) and Convergent sequence evolution between echolocating bats and dolphins (Liu et al. 2010) interpret what are very similar results, albeit for very dierent taxa, as parallel evolution of genetic
& 2011 Wiley Periodicals, Inc.

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changes in the case of C4 grasses, but convergent evolution of genetic changes in echolocating bats and dolphins. Furthermore, some view convergence at the molecular level as not being possible (Patterson 1988) others regard it as very rare (Castoe et al. 2009; Liu et al. 2010) others as occurring infrequently but diering from parallelism which is regarded as widespread (Zhang and Kumar 1997; Rokas and Carroll 2008), others that some level of convergence is common if not universal (Sanderson and Donoghue 1996; Bull et al. 1997) and by still others as being prevalent at the functional, mechanistic and structural levels, but maybe not the gene sequence level (Doolittle 1994). As a result, this issue constitutes much more than a semantic debate about appropriate terminology. Rather, it lies at the core of contemporary evolutionary biology and in particular, turns on how the patterns produced by the evolutionary process are described, characterized, and understood. This article focuses on several aspects of this issue from the perspective of homology, to ask whether any pertinent lessons can be gained from a consideration of convergence and parallelism from the perspective of that concept. Homoplasy and homology are terms that travel together (Wake 1996, p. xvii) because homoplasy is homology at a more restricted hierarchical level (Hall 2007).

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HOMOLOGY
Homology as an equivalence relation remains a term in general use in contemporary comparative biology (Scotland 2010 and references therein). Core aspects of homology are the conditional phrase (what is being compared) and the hierarchical level at which the comparison applies (Fig. 1). Bock (1974) suggested that any statement about the homology of features in dierent organisms must include a conditional phrase describing the nature of the relationship. The conditional phrase is partly determined by the variation of the parts being described and this, in part, is determined by the hierarchical level of the comparison (Fig. 1). The relation of homology is described as such because homology is a relational concept and because the degree of relationship varies, one must always state the nature or condition of a particular set of homologues (Bock 1974, p. 387). Although the conditional phrase and the hierarchical level can be considered as two separate aspects of homology determination, they are so interlinked as to encompass one idea or hypothesis. The alternative is to consider the conditional phrase as being independent and separate of the hierarchical level (either pre-Darwinian classications or explicit phylogenies). Such considerations are dicult to imagine from a systematic perspective, because character concepts for example carpels, nucleic acid, seeds, legumes, vertebrae, ns, amnion, etc., have been developed, rened, and conceptualized, hand

in-hand, alongside the context of hierarchy and classication and thus a specic hierarchical level (e.g., carpels of angiosperms, nucleic acids of life, seeds of spermatophytes, legumes of leguminosae, vertebrae of vertebrates, ns of shes, amnion of amniotes) and are therefore closely linked to the construction of predictive classications and/or, more recently, explicit phylogenies. In contemporary biology the taxic view of homology is rightly explained in terms of common ancestry and monophyly. Nevertheless the development and reciprocal illumination of character concepts alongside hierarchical groupings (taxa) has a creative, dynamic, and productive pre-evolutionary history. The taxic view of homology places great emphasis on the meaning, description, and interpretation of anatomy as interdependent with the hierarchical level. Other frameworks that emphasize comparative anatomy and development independent of hierarchy (Wagner 1989a, b) or alternatively promote hierarchies built upon operational character concepts (Sneath and Sokal 1973), have not been successful because it is the relationship between the twoFconditional phrase and hierarchyFthat provides insight and meaning. For example, Fig. 1 compares two fruits (one open and one closed) of Afzelia africana, in comparison with: (a) each other (b) fruits from the same family and (3) fruits from several families of owering plants. Although the fruit of A. africana, remains the same, the conditional phrase and abstracted homology is determined by the context of the comparisons that is the hierarchical level. Thus, the fruit can be categorized as: a type of legume relative to other individuals of the same species (A. africana); a fruit (legume) of the family Fabaceae; and a carpel of angiosperms. In this way hypotheses of homology comprise both an abstract conditional phrase and an explicit hierarchical level, for recent discussion see (Scotland 2010).

HOMOPLASY
Lankester (1870) is credited with introducing the term homoplasy as distinct from homology (which Lankester termed Homogeny) and provided the following example concerning the possible origin of the forms of weapons and utensils of various races of men to illustrate the distinction between homology and homoplasy. Lankester (1870, p. 41) wrote: Two races, A and B, without communication, may devise a stone axe or a canoe of similar forms: the resemblance is in this case homoplastic. Lankesters example includes two separate hierarchical levels (races) independently acquiring similar traits (axe and canoe). The homoplasy comprises part comparison (canoe and axe) and part hierarchical levels (races A and B). Homoplasies are therefore hypotheses of a correspondent trait that are distributed minimally at two separate hierarchical levels.

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The Relation of Homology

Conditional phrase Legume type

Hierarchical level Afzelia africana

what is this? In the comparative context of the objects on the right, it is a particular type of legume of Afzelia africana

Conditional phrase Legume

what is this?

Hierarchical level Leguminosae

In the comparative context of the objects on the right, it is a legume of the family Leguminosae

what is this?

Conditional phrase Hierarchical level Fruit Angiosperm

In the comparative context of the objects on the right and below, it is a fruit of an angiosperm.

Fig. 1. With reference to the specimen top left, or any biological specimen, we can ask, what is it? The answer (conditional phrase) depends on the hierarchical level of the comparison. (A) In comparison to a similar specimen from the same species, it is a particular type of legume of Afzelia africana. (B) In comparison to other fruits from the same family (Leguminosae/Fabaceae) it is a legume. (C) In comparison to other types of fruit, it is a fruit of angiosperms. Therefore the identity and meaning of a biological object is determined by the hierarchical level of the comparison which in turn determines the conditional phrase that is necessary to describe the object. Drawings of specimens from the Oxford University Herbarium (FHO) by Rosemary Wise. Fruits are from Afzelia africana, Gliricidium sepium, Enterolobium cyclocarpum, Castanopsis tibetana, Entandrophragma excelsum, Proboscidea althaeifolia, Jacaranda mimosifolia.

All homoplasy creates the same pattern, resulting in the independent occurrence of the same feature relative to phylogeny
In the phylogenetic specialist literature and textbooks, homoplasy is often described as having a number of possible explanations including convergence, parallelism and reversal (Hennig 1966; Page and Holmes 1998; Hall 2007, 2008). However, reversal of a character state causes the independent occurrence of the same character state in dierent places on the cladogram. As a consequence, reversals can and often are

viewed (Conway Morris 2003, 2010; Sucena et al. 2003) as a subset of either parallelism or convergence. For example, reversal to the plesiomorphic fusiform body shape in whales and dolphins compared with shes is a reversal that results in convergence (Conway Morris 2003) and independent loss of trichomes in dierent species of Drosophila are described as convergence (Sucena et al. 2003). Figure 2 illustrates this relative to an unrooted tree of seven taxa, three of which have the character state gray and four of which have an alternative character state black. The un-rooted tree shows that gray is a

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root 2 root 1

root 1

root 2

Fig. 2. Hypothetical unrooted tree showing the independent distribution of gray as homoplasy. Rooting the tree in two separate positions changes the scenario of character evolution but both phylogenies contain a convergent phenotype, generated by reversal/loss in rooting position 1 and independent gain in rooting position 2.

homoplasy. Rooting positions 1 and 2 both result in the independent evolution of gray relative to the phylogeny. The scenarios of character evolution leading to these convergences are dierent, but nevertheless both share the same patternFcorrespondent character state distributed at more than one hierarchical level. Therefore, all homoplasy creates the same general pattern; the separate occurrence/acquisition of a correspondent character state at more than one location on a phylogeny. In this sense, all homoplasy whether it be phenotypic or genotypic is equivalent: the recurrent tendency of biological organization to arrive at the same solution, (Conway Morris 2003, p. xii).

Four criteria for distinguishing parallelism from convergence

Homoplasy is considered by most biologists to include examples of both parallelism and convergence, but these terms are interpreted and used in a number of ways. For some authors for example Arendt and Reznick (2008a) parallelism and convergence are indistinguishable and the distinction between them is unnecessary and irrelevant. For others includ-

ing Arendt and Reznick (2008a) and Scott (1891, p. 363) the distinction between the two classes of phenomena is obviously one of degree rather than kind and for Simpson (1945, p. 9) the two phenomena intergrade continuously and are often indistinguishable in practice. Still other authors have distinguished between them on the basis of: (1) homoplastic character states that either correspond structurally (parallelism) or do not (convergence), (see Patterson 1982, 1988); (2) taxa sharing independent traits are either closely related (parallelism) or not (convergence), (see Scott 1896; Arendt and Reznick 2008a, b; Leander 2008), (3) Independent traits that share the same ancestral character states (parallelism) or not (convergence), (see Hennig 1966; Reidl 1979; Leander 2008); and (4) independent traits caused by the same underlying genetics or an ancestral predisposition (parallelism) or not (convergence), (see Haas and Simpson 1946; Brundin 1976; Gould 2002). These four criteria are listed in Table 1. The rst criterionFwhether the characters are really similar (structurally correspondent) or notF, refers, in part, to the distinction between analogy used in this article in a broad sense to distinguish all nonstructurally correspondent comparisons and all other relations including homology and homoplasy (Fig. 3). In much of the literature, both parallelism and convergence are regarded as forms of homoplasy in the sense of Lankester (1870) and consist of structurally correspondent traits distributed between at least two hierarchical levels (Fig. 3, Table 2). If convergence is restricted to independent traits that are noncorrespondent then this would be at odds with many examples and much of the widespread and general usage of this term in evolutionary biology. The second criterionFclose or remote relationships of the taxa bearing the charactersFis not relevant in the overall context of a comparative system that emphasizes the conditional phrase and hierarchical levels. This is because an explicit hierarchical level is much more precise and lacking in ambiguity compared with close or remote relationships of the taxa and the inevitable and endless discussion about just how close is close. Homoplasy and homology can be relevant at all hierarchical levels. The third criterionFwhether the characters have the same or dierent ancestral character statesFplaces emphasis not on the phenomenon under scrutiny (evolution of correspondent traits at two or more separate hierarchical levels), but on the underlying dierences at an altogether

Table 1. Four criteria identied in the literature to distinguish convergence from parallelism
1 2 3 4 Homoplastic phenotypes are structurally correspondent in parallelism but noncorrespondent in convergence Homoplastic phenotypes in closely related taxa is parallelism but in distantly related taxa is convergence Homoplastic phenotypes have the same ancestral character states for parallelism but dierent ancestral character states for convergence Parallelism comprises homoplastic phenotypes caused by the same underlying genetics resulting from an ancestral predisposition to evolve the same character states, whereas convergent phenotypes are caused by dissimilar genetics

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hypothesis of homology

analogy & homology sensu Owen 1843

Non- structural correspondence structural correspondence

more than one hierarchical level

one hierarchical level

Analogy sensu Owen 1843, non-homology sensu de Beer 1971, convergence sensu Patterson 1982, disparate morphology sensu Shubin et al 2009
Phenotype Analogy

Homoplasy sensu Lankester1870, usually interpreted as including convergence, parallelism, reversal and loss.

Homology sensu Patterson (1982) equivalent to synapomorphy (includes symplesiomorphy) at appropriate level.

Convergence

Homology

Genotype

Non-correspondence

Parallelism

Homology

Fig. 3. Schematic treatment for hypotheses of homology contrasting homology sensu Owen (1843) and homology sensu Patterson (1982). Putative hypotheses of homology are distinguished as analogy or homology in the sense of Owen (1843). Analogy is interpreted in a broad sense to include all nontopographically correspondent features including nonhomology sensu de Beer (1971) and disparate morphology sensu Shubin et al. (1997, 2009). Homology sensu Owen (1843) can be further divided into hypotheses of homology that are congruent with phylogeny at a particular hierarchical level and homoplasy that is incongruent with phylogeny. Some hypotheses that are congruent with phylogeny nevertheless have incomplete conditional phrases (ancestral character states) and dene paraphyletic groups. Structurally correspondent homology propositions that are congruent with phylogeny and dene monophyletic taxa are apomorphy (synapomorphy) or taxic homology sensu Patterson (1982). Two lower panels reect the framework adopted in this article for homoplasy. Convergence describes all phenotypic homoplasy and parallelism describes all genotypic homoplasy.

more inclusive hierarchical level, the plesiomorphic precursors of the independent traits. This criterion is at odds with some universally agreed examples of convergence that contradict this view because the convergent phenotypes have the same ancestral character states. For example, in the classic case of succulent desert plants of Cactaceae compared with succulent plants of the distantly related genus Euphorbia, the plesiomorphic conditions that led to both groups sharing structurally correspondent ridged and columnar stems are similar. Therefore, both the legitimacy and utility of distinguishing parallelism from convergence using criterion 3 is certainly far from universal. Furthermore, in a book devoted to convergence Conway Morris (2003) characterized hundreds of examples of convergence without any explicit focus on ancestral character states reecting the widespread use of this term without reference to ancestral character states. Thus, in agreement with many authors (Haas and Simpson 1946; Zhang and Kumar 1997; Wichman et al. 1999; Gould 2002; Cooper et al. 2003; Colosimo et al. 2005; Fong

et al. 2005; Harrison et al. 2005; Derome et al. 2006; Roberge et al. 2006; Shapiro et al. 2006; Christin et al. 2007; Hall 2007), criterion 4Fwhether similar independently evolved phenotypic character states have similar developmental mechanisms and genetics (parallelism) or not (convergence)Flies at the heart of the distinction between these categories. Criteria 13 are sometimes viewed individually or collectively as reecting, or acting as a proxy for, criterion 4. However, in the vast majority of cases, the validity of this assumption is, at best, loose and more typically, unknown.

Criterion 4, genetics and parallelism

Haas and Simpson (1946, p. 336) reviewed the distinction between parallelism and convergence and noted that parallelism would be similarity in structure due to a common genetic basis (and so far resembling homology) but not reaching morphological expression until after the separation of the two

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Table 2. Structural correspondence and hierarchical level distinguish noncorrespondent morphologies, homoplasy, and homology, but not parallelism from convergence
Structural correspondence Nonhomology Homoplasy: convergence Homoplasy: parallelism Homology No Yes Yes Yes Hierarchical level N/A At least two At least two One/unique

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or more lines involved (and in this diering from homology). Several other terms, (homoiologies, latent homology, underlying synapomorphy, unique inside-parallelism) have been used at various times to describe parallel evolution (Hennig 1966; de Beer 1971; Brundin 1976; Saether 1979, 1983, 1986). Hennig (1966) used the term homoiologies for corresponding characters that occur in narrow kinship groups but that nevertheless develop independently in their bearers. Saether (1983, p. 343) dened underlying synapomorphy as close parallelism as a result of common inherited genetic factors within a monophyletic group causing incomplete synapomorphy and Saether (1986, p. 5) as the inherited capacity to develop parallel similarities. de Beer (1971, p. 9) when discussing latent homology, thought that criteria for recognizing homology were perhaps over exacting because in many situations the manifestation of a homology was only visible or expressed in some of the taxa that shared the homology. These explanations of parallelism seek to explain a homoplastic morphological expression associated with a genetic mechanismFcommon inherited genetic factors and inherited capacity and community of inheritanceFthat is a genetic mechanism distributed at a more inclusive phylogenetic level than its associated homoplastic morphology. Gould (2002), in an extensive discussion of parallelism, makes the case that parallelism is an under-researched and important phenomenon within evolutionary theory. His arguement, partly rested on the results of evo-devo research that demonstrate a deep homology of shared genetics that underpin a range of phenotypic structures. Gould (2002) uses these examples to make the case for parallelism being channeled from within by homologous generators (Gould 2002, p. 1079) as the result of internal constraint (Gould 2002, p. 1080). Goulds treatment of parallelism states that its denition has been problematic: parallelism is a grey zone between homology and convergence but that criteria for its operational discovery, the operational rescue of parallelism by evo-devo and the development of genetic and developmental techniques that established the eld of evo-devo have nally allowed biologists to identify the homologous generators that always specied the

concept of parallelism in theoretical terms. Parallelism has now, and nally after a century of terminological recognition, become an operational subject for evolutionary research (Gould 2002, pp. 10881089). Gould was correct to highlight the huge potential of molecular biology to explore the relationship between the genotype and phenotype. However, this in itself does not provide a solution per se regarding the ambiguous use of the term parallelism, as the examples discussed below clearly demonstrate. A recurring theme in the discussions cited above is that parallel evolution of the same phenotypic trait which often but not exclusively occurs in closely related monophyletic lineages, represents something distinct from convergence, as the genetics and phylogenetic context (community of inheritance, homologous generators) that underpin parallel phenotypic homoplasies are more extensive than for convergent phenotypic homoplasies. This view would implicitly consider, analogy, convergence, parallelism, and homology as stages along a continuous spectrum from less to more shared genetics determined in part by the closeness of phylogenetic relations. In other words, analogies and convergences have few, if any genes in common whereas parallelism, and particularly homology, are both largely underpinned by the same genetic mechanisms. However, the view that homologous structures can be underpinned by nonhomologous genotypes and vice versa (de Beer 1971) coupled with recent discoveries that homologous genes can underpin widely disparate analogous morphologies (Panganiban et al. 1997; Shubin et al. 1997, 2009; Panganiban and Rubenstein 2002) calls this oversimplied view into question. In short, the concept of deep homology (Shubin et al. 1997, 2009) for examples in which the sharing of the genetic regulatory apparatus that is used to build morphologically and phylogenetically disparate animal features, has developed because analogous and homoplastic phenotypes can be regulated and determined by varying degrees of similar or dierent underlying genetics. The concepts of deep homology and parallelism are therefore closely related but both require precision in their use if they are to be more than a simple loose description of associated genotypic and phenotypic change.

A solution for use of the term parallelism

The criteria listed in Table 1 to distinguish parallelism from convergence may be unsuccessful because they treat these two ideas as mutually exclusive alternatives. But what if parallelism and convergence are not regarded as alternatives, but rather that the parallel evolution of genetic traits represents one of several possible types of explanation of phenotypic convergence. Under this model the parallel evolution of the same genetic traits can underpin and explain someFalthough not allFinstances of phenotypic convergence.

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Phenotype Non-homology Genotype Non-homology Relation / description Convergence

Biological levels
To appreciate the perceived distinction between parallelism and convergence it is necessary to understand the signicance of criterion 4Fwhether or not the characters have similar developmental mechanismsFin the wider context of the dissociation of homology (and homoplasy) propositions at various biological levels. de Beer (1971) was among the rst to point out that the expectation of homologous phenotypes being determined/regulated/specied by homologous genes/ genetic mechanisms was not always true. He provided several examples of homologous phenotypes and nonhomologous genotypes and vice versa, a view that has been explored widely (de Beer 1971; Roth 1984, 1988; Dickinson 1995; Bolker and Ra 1996; Galis 1996; Abouheif 1997, 1999; Abouheif et al. 1997; Shubin et al. 1997; Wray and Abouheif 1998; Wray 1999; Abouheif and Wray 2002; Hall 2003; Scholtz 2005; Sommer 2008, 2009; Shubin et al. 2009; Scotland 2010). Given the possible dissociation of hypothesis of homology (and homoplasy) at various biological levels that is genetic mechanisms, genes, and morphology (see Scotland 2010 for recent discussion), what lessons can be learned relative to criterion 4 from Table 1 for distinguishing parallelism from convergence? Focusing on two biological levelsFphenotype and genotypeFwithin a simplied framework of nonhomology, homoplasy and homology under the assumption that the hypotheses of phenotypic and genotypic homology can be disassociated, results in nine possible combinations (Fig. 4). Eight of these theoretical combinations could be pertinent, the exception being those of a nonhomologous phenotype and nonhomologous genotype. The association of a homoplastic phenotype as shown on the left hand side of Fig. 4, with the genotype on the right hand side, is reected by three arrows. Furthermore, whether the homoplastic phenotype has the same genetic mechanism (criterion 4), is reected by the two arrows pointing to homoplastic and homologous genotypes respectively. Because homologous traits of any type (genetic or phenotypic) dene monophyletic groups, it is logically impossible for the same genetic mechanism to characterize a clade as well as regulate a phenotypic convergence within that clade, reecting the fact that maybe all theoretical combinations in Fig. 4 are not possible. Therefore, the same genetic mechanism, associated with homoplastic phenotypes, must also be homoplastic. As a result, the black arrow that points between the homoplasy of the phenotype and homoplasy of the genotype fullls criterion 4. In this context, the terms convergence and parallelism describe the relationship between two biological levelsFphenotype and genotype. Convergence refers to the association between a homoplastic phenotype determined by nonhomologous genotype. Parallelism refers to the association between homoplastic correspondent genotypes determining homoplas-

Homoplasy

Homoplasy

Parallelism

Homology

Homology

Fig. 4. Two biological levels of organizationFphenotype and the genotypeFviewed relative to nonhomology (noncorrespondent comparisons), homoplasy, and homology. There are eight possible combinations of interest. A black arrow points to homoplastic phenotypes in combination with nonhomologous genetic mechanisms and this is considered by some authors (e.g., Haas and Simpson 1946; Gould 2002; Hall 2007) as convergence. A second black arrow indicates the combination of homoplastic phenotypes and homoplastic genotypes; this has been characterized as parallelism (e.g., Haas and Simpson 1946; Gould 2002; Hall 2007). The problem with this framework is that convergence is a widespread term referring to convergent phenotypes for which no genetic information exists.

tic phenotypes. If this distinction is accepted, one source of confusion between terms is that they are often used to refer to homoplastic phenotypes (left hand side of Fig. 4 only) in the hope that some aspect of the phenotype (not really the same, close or distance of the comparison, ancestral character states) can serve as a proxy for the genotypic information on the right-hand side of the diagram. This is mistaken because if phenotype and genotype can be dissociated, then no aspect of the phenotype predicts the condition of the genotype and vice versa. The obvious solution is to use the terms parallelism and convergence only when information exists for both phenotype and genotype, in which case they can then be used to describe the two biological levels relative to the independent acquisition of the same phenotype. The disadvantage of this solution is that it lacks the ability for either term to be used in a widespread manner when referring to the independent evolution of correspondent phenotypes. This is because the terms will now rarely be able to be used, as only rarely will the information required to distinguish them be available. Another solution is as follows. Parallel evolution has long been associated with the idea of shared genetic traits that underpin correspondent homoplastic phenotypes with the expectation that this phenomenon is more prevalent in closely related taxa (Haas and Simpson 1946). A possible resolution of this aforementioned dilemma, therefore, is to view parallel and convergent evolution not as alternatives, but rather parallelism as a possible explanation of phenotypic convergence. Parallel evolution of the same

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Phenotype Non-homology Genotype Non-homology

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Homoplasy Convergence Parallelism Parallel evolution

Homology

Homology

Deep homology

Fig. 5. Two biological levels of organizationFphenotype and genotypeFviewed relative to nonhomology (noncorrespondent comparisons), homoplasy, and homology. Convergence is restricted to one side of the diagram as it describes phenotypic homoplasy. Parallelism is restricted to one side of the diagram as it describes genotypic homoplasy. The conditional phrase associated with parallelism can refer to genotype only for example frequent and widespread parallel evolution of protein sequences Rokas and Carroll (2008) or genotype in relation to phenotype, C4 photosynthesis evolved in grasses via parallel adaptive genetic changes Christin et al. (2007), in which case it is an example of parallel evolution. Deep homology as originally proposed by Shubin et al. (1997, 2007) has a conditional phrase that combines nonhomologous phenotype and homologous genotype.

genetic traits can underpin and explain phenotypic convergence. In this framework (Fig. 5), convergent phenotypes refer to one biological level of homoplasyFthe phenotype. Parallel genetic traits refer to one biological level of homoplasyFthe genotype. Parallelism of genetic traits associated with a convergent phenotype refers to two biological levels of homoplasyFthe genotype and the phenotype (Fig. 5). Convergent phenotypes, however, have other explanations that do not rely on the independent parallel evolution of shared genetic traits or mechanisms. In summary, convergence can be viewed as a concept of phenotypic homoplasy, and parallelism viewed as a concept of genotypic homoplasy (see Figs. 3 and 5). These two separate hypotheses of homoplasy of phenotype and genotype can be combined such that shared homoplastic genetics can explain convergent phenotypes and therefore the genetics that underpin these concepts can be determined empirically rather than assumed from subsidiary problematic criteria (Table 1).

FOUR EXAMPLES

Example 1: pale and dark coloration in animals

In an article titled A single amino acid mutation contributes to adaptive beach mouse color Hoekstra et al. (2006) identied a derived, charge-changing amino acid mutation in the melanocortin-1 receptor (Mc1r) in light-colored subspecies of Peromyscus polionotus from the Florida Gulf Coast compared

with their dark-colored mainland conspecics. The same study reported that similarly light-colored subspecies from the Atlantic coast were missing the derived Mc1r light-colored allele, thus implying that dierent molecular mechanisms are responsible for the supercially convergent phenotypic evolution in light-colored subspecies from the Atlantic coast compared with the Florida Gulf Coast. This same gene (Mc1r) has also been implicated in the evolution of pale or dark coloration in lizards, several birds, various felids, pocket mice, black bear and woolly mammoths. In a discussion of parallel and convergent evolution, Arendt and Reznick (2008a) use the example from Hoekstra et al. (2006) to show that the distinction between parallel and convergent evolution is problematic. These authors reason that the distinction between convergent and parallel evolution assumes that, when a given phenotype evolves, the underlying genetic mechanisms are dierent in distantly related species (convergent) but similar in closely related species (parallel). However, studies of the Mc1r gene and coloration show that the same phenotype might evolve among populations within a species by changes in dierent genes (light-colored beach mice from the Gulf Coast compared with the Atlantic Coast), and conversely that similar phenotypes might evolve in distantly related species by changes in the same gene (lizards, birds, felids, pocket mice, black bear, and wooly mammoths). This led Arendt and Reznick (2008a) to the conclusion that the distinction between convergent and parallel evolution is a false dichotomy, at best representing ends of a continuum. They concluded that all instances of the independent evolution of a given phenotype can be described with a single termFconvergence. An interpretation of these data from the perspective of homology is as follows. In the example of P. polionotus, there seem to be three reasons why a particular group of individual mice share the light-colored trait. Either (a) the mice are light colored because they share a homologous genetic mutation inherited from light-colored parents (homology of trait and mechanism), (b) they share a genetic mutation of the same light-colored trait but both trait and mechanism have arisen in dierent individuals independently (homoplasy of both trait and mechanism), or (c) they share the light-colored trait but not the mechanism that determines the trait (homoplasy of trait and nonhomology of mechanism). These three scenarios are depicted in Fig. 6. Thus, this case can readily be accommodated within the framework outlined above, so long as the various hierarchical levels implied by the comparison are made explicit. The distribution of light pelage occurs at three independent hierarchical levels, two in the Florida gulf coast and one in the Atlantic coast. This phenotypic trait is a homoplasy. The answer to the convergence/parallelism question depends on the same qualications as any other example of homology or homoplasy; on the hierarchical and biological level of the focus. Relative to Fig. 6, the presence of light pelage is homologous (apomorphic) at three separate

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evolution of the same genetic mechanism that has a role in determining a convergent phenotype. The evolution of white pelage in various subspecies of mice from the Florida gulf coast compared with the Atlantic coast can be described as convergent evolution of a phenotype.

phylogenetic levels (FG, MN, and WZ) and homoplastic within the level of AZ, (at three independent levels). Within the level of EN, light pelage is homoplastic and this homoplasy is determined by the independent evolution (homoplasy) of the same genetic mechanism (parallelism of genetic mechanism in relation to a convergent phenotype). In addition, comparison of light pelage at levels FG or MN compared with WZ is homoplasy that is determined by the independent evolution of a phenotype determined by dierent genetic mechanisms (convergence of phenotype). In describing this example, I was reminded of the classic textbook example concerning whether the wings of birds and bats are homologous. The ocial answer is that the wings of birds and bats are homologous as forelimbs at the level of tetrapods, homoplastic as wings at the level of tetrapods, and homologous as particular types of forelimb at the levels of birds and bats respectively. These interpretations depend solely on the hierarchical level of the comparison. This is the case within any cladeFa species, a genus, or all of life. Therefore, the evolution of light pelage in Florida gulf coast mice, lizards, birds, felids, pocket mice, black bear, and woolly mammoths involving the Mc1r are all examples of parallel

Example 2: echolocation in bats and dolphins

In an article titled Convergent sequence evolution between echolocating bats and dolphins, Liu et al. (2010) demonstrated that the motor protein Prestin expressed in mammalian outer hair cells has a role in echolocation in bats and dolphins. The ability of some bats and all toothed whales to produce sonar pulses and process the returning echoes for prey detection and orientation (echolocation) is described as a spectacular example of phenotypic convergence in mammals. These authors demonstrate that echolocating whales and bats uniquely shared 14 derived amino acids in the Prestin protein. Using the full amino acid alignment of the Prestin protein these authors infer a phylogenetic tree that has the echolocating whales nested within bats due to homoplastic evolution of the shared amino acids (Fig. 7).

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dark pelage light pelage derived Mc1r allele determining light pelage unknown genetic mechanism

Florida gulf coast and mainland

U V W X Y Z

Atlantic coast and mainland

Fig. 6. Hypothetical phylogeography of subspecies of Beach Mouse Peromyscus polionotus distributed in the Florida gulf coast and the Atlantic coast. The tree shows that light pelage (coat color) has evolved three independent times. Two of these occurrences are found in mice in Florida and it has been shown that this is determined by the derived Mc1r allele. Another set of mice on the Atlantic coast do not share this allele and therefore the light pelage in these mice is determined by another, unknown genetic factor. Light pelage is a convergence (three levels) at the level of AZ and homology at the independent levels of FG, MN, and WZ. The convergent light pelage at the level of BN is explained by the parallel evolution involving Mc1r whereas the convergence between light pelage in the Florida gulf coast and Atlantic gulf coast remains as convergence. Illustrative phylogeny to capture discussion presented in Arendt and Reznick (2008a) and Hoekstra et al. (2006).

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onstrated that the same parallel, putatively adaptive genetic changes were associated with the independent evolution of C4 photosynthesis in grasses. Excerpts from the abstract of this article are very instructive in relation to the precise use of the terms parallelism and convergence (Christin et al. 2007, p. 1241).
Phenotypic convergence is a widespread and well-recognized evolutionary phenomenon. However the responsible molecular mechanisms remain often unknown mainly because the genes involved are not identied. A well-known example of physiological convergence is the C4 photosynthetic pathway, which evolved independently 445 times. Here we address the question of the molecular bases of the C4 convergent phenotypes in grasses (Poaceae) by reconstructing the evolutionary history of genes encoding a C4 key enzyme (PEPC). . . . Using phylogenetic analysis we showed that grass C4 PEPCs appeared at least eight times independently from the same non-C4PEPC (Fig. 8). Twenty-one amino acids evolved under positive selection and converged to similar or identical amino acids in most of the grass C4PEPC lineages.

Toothed echolocating whales

Echolocating bats

Fruit bats Cow Correct position for toothed echolocating whales

baleen whales Human

These authors concluded that C4 photosynthesis evolved in grasses via parallel adaptive genetic changes using the term convergence to refer to homoplastic phenotypes and their usage of parallelism is restricted to parallel genetic changes associated with this convergent phenotype. As a result this usage is in agreement with the framework developed in this paper.

Fig. 7. Evidence of sequence convergence in the Prestin gene between dolphins and bats. Phylogeny based on amino acid data. Tree shows echolocating toothed whales (dolphins) nested within bats. Gray line indicates the correct position of toothed whales. Echolocation is convergent for some bats and dolphins and evolves via parallel changes in sequence evolution of the Prestin protein. Modied and redrawn from Liu et al. (2010).

Example 4: Drosophila trichomes

The abstract of a compelling article entitled Regulatory evolution of shavenbaby/ovo underlies multiple cases of morphological parallelism (Sucena et al. 2003, p. 935) is as follows:
Cases of convergent evolution that involve changes in the same developmental pathway, called parallelism, provide evidence that a limited number of developmental changes are available to evolve a particular phenotype. To our knowledge, in no case are the genetic changes underlying morphological convergence understood. However, morphological convergence is not generally assumed to imply developmental parallelism. Here we investigate a case of convergence of larval morphology of insects and show that the loss of particular trichomes, observed in one species of the Drosophila melanogaster species group, has independently evolved multiple times in the distantly related D. virilis species group. We present genetic and gene expression data showing that regulatory changes of the shavenbaby/ovo (svb/ovo) gene underlie all independent cases of this morphological convergence. Our results indicate that some developmental regulators might preferentially accumulate evolutionary changes and that morphological parallelism might therefore be more common than previously appreciated.

There seems little doubt in this example that echolocation and associated morphological traitsFshorter and stier cochlear outer hair cellsFare homoplastic in mammals. The question is whether this represents convergent or parallel evolution. Following the framework developed above, the shared echolocating phenotype of bats and dolphins and the shared amino acids of the Prestin protein are both homoplasies and can be described as the same phenotype evolving independently using the same genetic changes. Replacing the word convergence with parallelism in the title of the article would more accurately describe these data. In other words, parallel evolution of the Prestin protein is associated with phenotypic convergences involved in echolocation in mammals.

Example 3: C4 photosynthesis in grasses

In a article entitled C4 photosynthesis evolved in grasses via parallel adaptive genetic changes, Christin et al. (2007) dem-

The conceptual framework of Sucena et al. (2003) comprises morphological convergence and parallel developmental pathways to explain those morphological convergences. The authors conclude however that morphological parallelism is perhaps more common than previously appreciated. These

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L V

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Fig. 8. Grass phylogeny with bold branches corresponding to C4 species and nonbold branches C3 species. Colored panel of 12 amino acid positions from the C4 key enzyme PEPC, showing parallel evolution to the same amino acids in the C4 taxa. C4 photosynthesis evolved in grasses via parallel adaptive genetic changes. Black arrows correspond to C4 taxa. Modied and redrawn from Christin et al. (2007).

authors seek to reinterpret cases of morphological convergence as morphological parallelism, when it can be shown that the same genetics underpin the independent evolution of the same phenotype. A simpler and more straightforward interpretation of these data is that the convergent evolution (loss of trichome) of the same phenotype can be explained by parallel evolution of svb regulatory mechanism (Fig. 9).

DISCUSSION AND CONCLUSIONS

Homology and homoplasy are terms used to describe the distribution of correspondent traits relative to phylogeny. Just as homology is associated with descriptive terms such as unique innovation and evolutionary novelty, homoplasy is associated with a plethora of terms such as loss, reversal, parallelism and convergence. Relative to homoplasy however,

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D. kanekoi

D. ezoana

D. littoralis

D. borealis (Eastern) D. borealis (Western)

D. lacicola

D. montana

D. flavomontana
Fig. 9. A phylogeny of selected species of Drosophila presented by Sucena et al. (2003). The authors interpretation was of loss of trichomes on three separate occasions (black bars) resulting in convergent phenotypes. The authors demonstrate that parallel changes in the shavenbaby/ovo gene underly all three independent cases of loss of trichomes. Redrawn from Sucena et al. (2003).

this issue can be simplied because the common pattern of all phenotypic homoplasy is convergence and genotypic homoplasy is parallelism the equivalent term for molecular data. Just as homology has a number of explanations and causes (Van Valen 1982; Shubin et al. 1997, 2009; Wagner and Lynch 2010), so too is convergence associated with a number of possible causes, explanations and associations that is reversal, loss, parallel genetic changes, nonhomologous genetic changes, near and distant relatives, ancestral and non-ancestral character states, positive developmental constraint, functional convergent trait shaped by natural selection, etc. The relative extent of these various associated phenomena can be determined empirically if the underlying phylogenetic pattern is discovered independent of anyone particular association or

process. In other words, the description of phenomena and terms that refer to an explanation of phenomena should be distinctFdistinguishing the explanans from the explanandum (Brady 1985)Fand confusion and inconsistency regarding which of these a term refers to, are at the root of many controversies in biology (e.g., Gould and Vrba 1982). The view presented in this article provides a simplied framework for what evolutionary and developmental biologists have to explain in terms of comparative anatomy: the unique evolution of correspondent traitsFnovelty/synapomorphyFand the evolution of independent traitsFconvergence or its molecular equivalent parallelismF(Fig. 3). This clarication of the use of the terms convergence and parallelism involves restricting convergence to describing the independent evolution of correspondent phenotypes and view parallelism as describing the homoplasy of genotypes (Figs. 3 and 5). These two levels of homoplasy from the phenotype and genotype can then be combined to describe parallel evolution that is parallel genetic traits that underpin or are at least associated with phenotypic convergence. Convergence is about phenotypes, whereas parallelism, just like deep homology, is a conditional phrase that attempts to describe the relationship between genotype and phenotype. Convergent evolution involves one hypothesis whereas parallel evolution of genetic traits that underpin convergence of the phenotype, comprises two. When the term parallelism is restricted to all instances of genotypic homoplasy ( 5 the genotypic equivalent of phenotypic convergence), the meaning of parallel evolution becomes clear and unambiguous. One possible objection to this framework is that the use of the term parallelism to describe all genotypic homoplasy is too broad and that parallel genetic traits should be distinguished from genetic traits due to convergence and reversal. Rokas and Carroll (2008) distinguish molecular substitutions due to reversal to the pleseiomorphic state, convergence from dierent ancestral states and identical parallel changes to the same state, whereas Bull et al. (1997) adopted a broad view of convergence to describe all genotypic homoplasy. Despite terminological dierences, these studies (Bull et al. 1997; Rokas and Carroll 2008) are clear in their use of these terms. If parallelism is a term used to describe all instances of genotypic homolpasy, there is no reason why the shared presence of the same or dierent ancestral character states cannot be explicitly part of that framework where appropriate. The widely dierent use of these termsFconvergence, reversal, and parallelismFto describe dierent facets of molecular homoplasy at the DNA and amino acid sequence level conveys the impression that most authors dont distinguish fundamentally dierent underlying processes. In conclusion, Arendt and Reznick (2008a) were correct to highlight the confusing and ambiguous use of the terms parallel and convergent evolution that pervades the evolutionary literature. They were also correct to demonstrate that both

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similar and dierent genetic mechanisms can be associated with very closely related convergent phenotypes. I also agree with those authors that all instances of the independent evolution of a given phenotype can be described with a single termFconvergence. However, Arendt and Reznicks starting point, that parallelism and convergence were separate and distinct concepts primarily distinguished on close or remote relationship of the taxa, is not an accurate nor full characterization of the manner in which these terms have been used in the literature of evolutionary biology. It was their use of this incomplete framework that led them to conclude that the two supposedly distinct ideas could not be distinguished and, as a result, suggest that one termFconvergenceFsuces to describe independent evolution of phenotypes. I consider this to be mistaken, because the independent evolution of genetic traits (parallelism) that underpin or are at least associated with convergent phenotypes, is an increasingly active area of research and has become a well characterized phenomena (Sucena et al. 2003; Harrison et al. 2005; Christin et al. 2007; Liu et al. 2010). Adopting the view that parallel evolution of genotypes can explain or is at least correlated with some but not all convergent phenotypes accommodates the ultimate convergence of Leander (2008), the main arguments presented by Arendt and Reznick (2008a) and Gould (2002), as well as providing a conceptual framework for several examples from the recent literature (Hoekstra and Nachman 2003; Sucena et al. 2003; Hoekstra et al. 2006; Christin et al. 2007; Liu et al. 2010).
Acknowledgments
I thank Richard Bateman, Maxim Kapralov, Ian Kitching, Norman McLeod, Bill Wickstead, Brian Hall, and Rudi Ra for comments on the manuscript. Thanks also to Pascal-Antoine Christin who provided help with Fig. 8 and Angela Hay who helped with Fig. 1. Thanks to Miltos Tsiantis for many thought-provoking and interesting discussions about parallelism.

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