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Molecules and Morphology: Where's the Homology?

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Molecules and Morphology: Where's the Homology? COMMENT Molecules and morphology: where's the homology? W.J. DICKINSON DEPARTMENTOF BIOLOGLUNIVERSITY OF UTAH,SALT LAKE CITY, UT 84112, USA. A few years ago l, molecular biologists have also been considered (at least early speculations centered on the were chastised for sloppy and con- implicitly). If doubt remained, se- possibility that insects and vertebrates fusing use of the term 'homology'. quence data could be collected to share a conserved mechanism of Many treated homology as an objec- confirm that bats descend from wing- segmentation, even though this con- tive observation rather than an in- less mammals. tradicted the conventional view that ference, and as a quantitative trait Now, suppose the molecular the last common ancestor of arthro- ('percentage homology') rather than mechanisms controlling develop- pods and vertebrates was not seg- a relationship of common evol- ment in birds and bats are examined. mented. However, the discovery of utionary origin that either does or Given the known conservation of homeobox clusters in unsegmented does not exist (see description of mechanisms in vertebrates, homolo- creatures like Caenorhabditis elegans terminology in Box 1). There is gous molecules and conserved path- undermined these speculations, par- another source of confusion that ways would certainly be found oper- ticularly since analyses of expression threatens to become increasingly ating in the development of wings patterns in the worm confirmed that troublesome as the fascinating mol- in both groups. However, such simi- there is no relationship between ecular homologies that lie at the heart larities would not be interpreted homeobox genes and reiterated cell of developmental mechanisms are as supporting the surprising' con- lineages that might be regarded as a unraveled: there is not necessarily a clusion that the two sorts of wings are, primitive form of segmentation 8,9. simple relationship between hom- after all, homologous. Instead, the Homeobox genes are involved in ology of molecules (or even path- molecular similarities would be other divergent processes such as ways) and homology of the anatomi- recognized as reflecting homology at limb development in vertebrates 1° cal features in whose development a deeper level (forelimbs). In other and gut differentiation in insects1( those components participate. In studies, the danger arises when Thus, the focus of interpreting other words, some recent suggestions evidence beating on homology is less homeobox gene function shifted notwithstanding v7, molecular simi- extensive or decisive (or less well progressively from segmentation to larities in the developmental mech- known to the average molecular or anterior-posterior polarity lz and to anisms that produce specific organs developmental biologist) than in this axial patterning in general 13. Hom- are not, by themselves, strong evi- example. ology at even deeper levels, such as dence for homology of those organs. positional information per se or Interpreting homeobox gene simply transcriptional regulation, may Levels of homology comparisons be most relevant to some homeobox The central point of this article is Turning to real molecular ex- gene comparisons. that questions of homology can be amples, the evolving interpretation of A cautious initial interpretation of examined at multiple levels and that comparisons between homeobox similarities among insects and ver- homology between a pair of struc- genes and clusters in different organ- tebrates would have considered all tures can simultaneously be present isms is instructive. When these were of these possibilities and recognized at some levels but absent at others. discovered in vertebrates following the need for additional information to The term 'levels of homology' refers their initial characterization in insects, distinguish between them. As in the to a nested series of progressively more ancient and inclusive ('deeper') relationships. The classic textbook Box 1. Addendum on terminology example of homology, the vertebrate The terminology used in this article to describe rehtionships is that proposed by forelimb, conveniently illustrates the Fitch16, elaborated by Patterson17, and summarized in the instructions to authors point. Considered only as forelimbs, writing for Molecular Biology and Evolution. Briefly, features (including mol- the wings of birds and bats are ecules) that are similar by virtue of common ancestry are homologous, while homologous; considered as wings, those that are similar by convergence are analogous. Among homologous mol- they are not. In other words, the last ecules, those produced by gene duplication are paralogous and those separated common ancestor of these two by speciation are orthologous. It is possible (and useful), as Patterson suggests, to groups had forelimbs but not wings. give precise definitions even when there are substantial practical difficulties in Note that this conclusion is partly deciding which relationship applies in particular cases. There is, however, one based on evidence other than that problem of definition not dealt with in the cited sources. When duplication pro- cluces a paralogous gene set in one species,- is the orthologous relationship to derived from the direct comparisons homologs in other lineages retained by both, one, or neither of the copies? If it "is of wings: the comparative anatomy of retained by only one c0py, to which copy.sl~ould the orthologous relationship be other vertebrate forelimbs; the fossil assigned? This difficulty does not need to be resolved for the present purpose but record; and other anatomical com- it further highlights the complexities of using molecular similarities as evidence for parisons that reveal, for exaraple, the anatomical homology. relationship of bats to other- ,l~ammals TIG APPalL 1995 VOL. 11 NO. 4 @ 1995 Elsevier Science Ltd 0168 - 9525/95/$09.50 119 COMMENT example of bird and bat wings men- u'aced backwards from the current As with other developmental regu- tioned above, more detailed analyses examples under consideration. Such lators, these factors belong to a lim- of the relevant systenxs would not, in an analysis would identify the level at ited number of families and typically isolation, have resolved the question. which the contemporary functions function in a variety of contexts. The progressive interpretation sum- and contexts could usefully be said to Again, coincidental similarities be- marized above depended on in- be homologous. tween analogous systems are to be fom~ation about additional species expected. This case is also confused (e.g.C. elegans) and other contexts of Some questionable cases by the seemingly interchangeable use expression within species (e.g. limbs Molecular similarities have some- of the terms 'homology' and 'analogy' and guts); in turn, those comparisons times not been interpreted in an in file discussion. depend, at least implicitly, on ad- appropriately cautious manner. Laufer and Marigo 4 summarize ditional data of various kinds (such as Based on comparisons of function additional examples in which con- that relevant to phylogeny). and expression of the orthodenticle nections between molecular and gene in Drosophila and of homologs anatomical homology have been Homologous molecules in in vertebrates, Finkelstein and considered. The issues raised in this analogous orgam Boncinelli 2 suggest that, contrary to article have not always been given A second example highlights prevailing opinion, head specializ- adequate attention. It is noteworthy the classic problem of convergence, ation may have occurred before the that the majority of 'surprising' ana- with the deceptive twist that truly ancestral lineages separated. How- tomical homologies thus far pro- homologous molecules may be ever, the facts permit hypotheses posed on the basis of molecular data involved in processes that are only similar to those proposed for inter involve comparisons between insects analogous. Products of the hedgehog preting analyses of homeobox genes and vertebrates. This certainly reflects gene in Drosophila and of an avian mentioned above: these ortho- the intense effort devoted to molecular homolog serve strikingly similar func- denticle homologs could be deeply analyses of development in these par- tions in wing development 14. Quite conserved components involved in ticular systems. As other groups re- properly, their roles in that context axial patterning (or another aspect of ceive more attention, the incidence of are recognized as analogous, not positional information) not specifi- convergent examples will surely in- homologous. Again, hedgehog hom- cally related to cephalization. crease, reinforcing the importance of ologs play comparable roles in inter- Defects caused by eyeless in caution and precision in the interpret- cellular signaling in various other Drosophila and a homolog, Small eye, ation of molecular similarities. developmental contexts in both in mice have prompted speculation insects and vertebrates. Undoubtedly, that arthropod and vertebrate eyes Conclusions there is deep and interesting hom- are homologous despite fundamental In no case am I arguing that ology here but the wing is not the differences in organizationS,7. This suggested inferences about organ- level at which it should be sought. situation may be comparable to that level homology are definitely wrong; The probability of encountering of the hedgehog gene in wing de- I claim only that the molecular such convergence is greatly increased velopment. The roles
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