© 2000 by The Society for Integrative and Comparative Biology
Intraspecific Variation in Developmental Characters: The Origin of Evolutionary Novelties1
1 Ecology Centre, University of Sunderland, Sunderland SR1 3SD, United Kingdom
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Evolutionary developmental biology is inevitably a comparative subject. However, the taxonomic level at which comparisons can be made varies widely, and this greatly affects the kind of information that can be gained from the comparison. Broadly speaking, high-level comparisons (e.g., between phyla) are more informative about phylogenetic pattern and homology, while low-level comparisons (e.g., between congeneric species) are more informative about evolutionary mechanisms, including speciation. However, so far evolutionary developmental biology has had a relatively minor input into the traditional territory of population genetics, namely comparisons within species—both within and between geographic populations. Yet this area is crucial, as all evolutionary novelties ultimately arise from intraspecific variation. Here, I address this issue, focusing on the question of how early in development novelties arise. To shed light on this question, I discuss two examples of developmental polymorphism within species involving two of the main body axes: anteroposterior segmentation in centipedes and left–right asymmetry (chirality) in gastropods.
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INTRODUCTION |
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Over the course of evolutionary time, novelties of some sort or other ultimately arise in all lineages. A few of them will be major, many trivial. In the morphological domain, examples of novelties include the origin of feathers (Brush, 1996
), new cusp patterns in mammalian teeth (Hunter and Jernvall, 1995; Jernvall, 2000) and altered numbers of antennule segments in copepod crustaceans (Galassi and De Laurentiis, 1997). These are just a few of very many examples in the literature that are explicitly discussed as novelties. In general, the usage of "novelty" (or its synonym "innovation") has approximately doubled in volume over the last decade or so, as electronic searches readily reveal, reflecting the marked increase in interest in this topic that has occurred in the evo-devo era.
Although the origin of novelties can be taken for granted, and although countless examples can be given, there is no universally accepted definition of evolutionary novelty, and those definitions that have been attempted often conflict with each other. For example, Mayr (1963, p. 602) defines a novelty as "any newly acquired structure or property that permits the performance of a new function, which, in turn, will open a new adaptive zone." In contrast, Müller and Wagner (1991, p. 243) define a (morphological) novelty as "a structure that is neither homologous to any structure in the ancestral species nor homonomous to any other structure of the same organism." Clearly, these definitions specify groups of features that only partially overlap. Also, in my view, both definitions are too restrictive. Here, I will instead follow the more inclusive approach where novelties and apomorphies are regarded as essentially the same. (See, for example, Lee [1998] who refers to a synapomorphy as "a shared evolutionary novelty.")
The key question I focus on herein is whether morphological novelties that are large and obvious in the adult are the result of modification of early development. I have previously put forward the hypothesis that there is a statistical but not absolute link between earliness of onset in development and magnitude of change in the adult: the "cone model" (Arthur, 1997). The examples discussed in the present paper—changes in centipede segment number and switches in gastropod chirality—lend support to this idea, but there is an important caveat relating to heterochrony. If character state X1 (original) changes to X2 (new) at developmental time t1, this can be described as "early." If, instead, the shift occurs at t2, this can be described as "late." But there is another, heterochronic, possibility: from X1 at t1 (or t2) to X2 at t2 (or t1). Here, it is impossible to classify the change as either early or late. As we will see, switches in gastropod chirality are unambiguously "early." Changes in centipede segment number, however, are more heterogeneous in this respect. The shift from anamorphic to epimorphic groups (see below) involved the addition of segments plus a major heterochronic change from late to early development of the full complement of segments. In contrast, the evolution of new segment numbers within the derived epimorphic groups has always involved early developmental changes.
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INTRASPECIFIC VARIATION |
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Herein, I take it as axiomatic that anything we describe as a major novelty must, like other more minor evolutionary changes, have its origin in intraspecific variation. This variation may be persistent or fleeting. In either event, at the phenotypic level it can take any one of three well-known forms—continuous, meristic, or polymorphic (discrete).
The examples of novelty that I discuss below tend to fall into the polymorphic category. However, there is a complication in the case of segment number. If the number of segments varies over only two or three values within a species, then the variation is polymorphic. However, if it varies over (say) fifty values then it may be more appropriate to consider it as meristic. Since examples of both are known in centipedes, respectively Brachygeophilus truncorum (Arthur and Blackburn, 1999) and Hymantarium gabrielis (Minelli, et al., 1984), along with a spectrum of intermediates, the business of categorizing particular cases is not straightforward.
The relationship between developmental and genetic polymorphism deserves a brief mention here. In both cases, "polymorphism" refers to the simultaneous existence, in the same population, of discretely different forms. In genetic polymorphism, these are usually different alleles at a given locus. In developmental polymorphism, they are different morphological forms—e.g., different segment numbers. In some cases of genetic polymorphism (e.g., most allozymes: see Kimura, 1983), there is no corresponding developmental polymorphism, because the genes concerned have a housekeeping, not developmental, role. Equally, some cases of developmental polymorphism are not underlain by genetic polymorphism, because the different forms are ecophenotypic (or "plastic") in origin. Where developmental polymorphisms are indeed heritable, a relationship with genetic polymorphism necessarily exists but may be simple or complex, depending on whether the two or more morphological forms have their origin in allelic variation at a single major-effect locus or in a more complex, polygenic system. Gastropod chirality is an example of the former (see below). Centipede segmentation may well be an example of the latter, but this remains to be established.
The approach taken below in relation to both examples is to compare the phylogenetic distributions of (a) clades characterized by particular novelties and (b) the existence of related intraspecific variation, in the form of developmental polymorphism. This approach reveals the extent to which the two can be connected and, complementary to this, the difficulties that remain in attempting to understand how novelties arise.
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CENTIPEDE SEGMENT NUMBER |
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Phylogenetic pattern of the number of segments
There are approximately 3,000 species of centipedes (Class Chilopoda). Their trunk segment number ranges from 15 to 191—see reviews by Minelli and Bortoletto (1988)
and Arthur (1999)—"trunk segment" being synonymous with "leg-bearing segment." The 3,000 species belong to five extant orders, each characterized by a particular fixed number or variable range of trunk segments, and their pattern of relationship is shown in Figure 1. This pattern, in which the long, thin, subterranean geophilomorphs are derived, is the opposite of the pattern which found favour before a cladistic approach was used, in which the geophilomorphs were considered to be primitive. However, the pattern shown in Figure 1 now appears to be well founded, as it has been produced independently through three morphological cladistic analyses (Dohle 1985; Shear and Bonamo, 1988; Borucki, 1996) and one molecular cladistic analysis (based on rDNA: Giribet et al., 1999; Edgecombe et al., 1999). It should be noted that Shear and Bonamo (1988) describe an extinct sixth order of centipedes—Devonobiomorpha—but due to the fragmentary nature of the specimens it is not possible to ascertain their number of trunk segments.
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Curiously, the number of trunk segments in centipedes is always odd (Minelli and Bortoletto, 1988
; Arthur and Farrow, 1999). However, it is possible that the total number of segments is always even. Certainly, the "trunk" in a broad sense can be considered to include the forcipular (=poison claw) segment (add 1 to all numbers shown in Fig. 1). Also, it is possible that the head and genital areas, taken together, constitute a further 8 segments (add 9 to all numbers shown in Fig. 1). Further, it may be that segment anlagen are produced in a multiplicative manner, with the result that the final number of total segments is always even.
Minelli and Bortoletto (1988) devised an "octonary" model in which each initial primordium in early development is thought to give rise to 8 segments. Variation in the number of such primordia might explain a large part of the pattern shown in Figure 1. Starting with a craterostigmomorph-like ancestor, addition of a single primordium would cause a shift from 15 to 23 (scolopendromorph), while a further such addition would cause a shift to 31 (geophilomorph), and subsequent additions could take the number of segments to progressively higher numbers within the geophilomorph range. Variation at a later developmental stage would then be responsible for the smaller shifts involved in producing 21-segment scolopendromorphs (assuming these to be derived, though this is currently unclear), and "non-octonary" geophilomorphs.
It is apparent from Minelli and Bortoletto's (1988) presentation of the data that the pattern of distribution in many families of geophilomorphs shows an excess of octonary forms, which supports their model. (Note that a somewhat different model involving "meromeric" segmentation has recently been suggested by Minelli [2000].) So one possible picture of the evolution of centipede segment number is of very occasional "macromutational" shifts of 8 segments with, superimposed on that, more frequent smaller shifts of 2 segments in the Scolopendromorpha and, especially, the Geophilomorpha (where it is possible that shifts of 4 segments also occur).
Intraspecific variation
Intraspecific variation in segment number occurs only in the Geophilomorpha, and so is itself a novelty of that group. (The only exception is the geophilomorph family Mecistocephalidae, whose species are invariant and which may be the cladistic outgroup to the rest of the order: Foddai 1998). It is thus the Geophilomorpha that provides possible model systems for studying the link between intra- and inter-specific variation. An example of how congeners vary in trunk segment number is given in Table 1 for British species of the genus Geophilus (compiled from Eason 1964). As can be seen, some species overlap extensively while others (e.g., G. electricus) stand alone in that they show no overlap of values with the other species. This suggests that some speciation events involve no shifts in segment number, others slight shifts, yet others major shifts (perhaps again by 4 or 8 units).
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Closely related to Geophilus is the genus Strigamia, one of whose member-species, S. maritima, is particularly abundant and thus provides an unusual opportunity to study intraspecific variation. (Most geophilomorphs are rare, and it is hard to obtain workable sample sizes.) It has been known for some time that different populations of S. maritima differ significantly in their segment number. Recently, it has also become apparent that there is a geographic pattern to the variation, involving a decrease in segment number with increasing latitude (Kettle and Arthur, 2000
). Given that there appears to be a high heritability of segment number in geophilomorphs (Prunescu and Capuse, 1971), it is not hard to envisage a typical allopatric speciation scenario, with geographically isolated populations diverging in a suite of characters including both segment number and reproductive compatibility. There is, however, a problem. The most impressive novelty that occurred in the evolution of centipede segment number is the +8 (or possibly +6) shift that led to the origin of the scolopendromorphs. This appears to have occurred as a single evolutionary step in that neither living nor fossil intermediates are known between the character states 15 (lithobiomorphs) and 21/23 (scolopendromorphs). If this is so, then the shift was probably based on a very fleeting variation within a single ancient stem species, rather than on widespread, persistent intraspecific variation such as characterizes present-day geophilomorphs. It is thus questionable to what degree the Geophilus/Strigamia model applies to the origin of such a novelty.
This problem of the non-correspondence of the most interesting (=major?) and the most studyable (=minor?) novelties is a frequent occurrence. It can be viewed as yet another manifestation of the awkwardness, or cussedness, of organisms. Park (1939) refers to the Harvard Law of animal behaviour, namely that "animals under the most precisely controlled laboratory conditions do as they damn please." I would like to add to this the Atlanta Law of the evolution of development: "The most interesting evolutionary novelties are the hardest to study."
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GASTROPOD CHIRALITY |
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Phylogenetic pattern of sinistrality/dextrality
Clearly, Gastropoda is a much more speciose clade than Chilopoda—some 50,000 species as opposed to a mere 3,000. The internal phylogeny of this vast group is not yet well established. (There is currently at least one molecular phylogeny study under way [B.C. Clarke, personal communication], and its results are awaited with interest.) I will therefore take a slightly different approach than with centipedes and, instead of attempting to produce an overall phylogeny, I will follow Robertson's (1993)
approach of treating superfamilies as monophyletic units within which to look at the distribution of dextral and sinistral forms. I will be very selective, using just a few superfamilies for illustrative purposes (Table 2, Fig. 2), and ignoring the question of how they are inter-related. (They are thus shown as an unresolved polytomy in Fig. 2.)
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The five superfamilies shown in Figure 2 depict the five kinds of clade found with respect to the occurrence of sinistrals and dextrals: sinistrals only; majority sinistral; very heterogeneous; majority dextral; dextrals only. There are almost 100 gastropod superfamilies in total, and the vast majority of these fall into the last two categories, reflecting the very pronounced dextral bias that is known to characterize Gastropoda.
The Partuloidea stand out, among the gastropods, as an unusually variable group. Partula itself has been studied most intensively (see review by Johnson et al., 1993). There are dextral species, sinistral species, and a variable species (P. suturalis—see below) all within the same genus. Indeed, the delineation of species boundaries is not entirely clear, and the number of named species of Partula has altered markedly (downwards for the most part), as ideas have shifted on whether particular forms represent independent species or part of a species-complex.
Gastropod chirality is unlike centipede segmentation in that there has not been a general trend in one direction. Rather, it appears that chirality is highly constrained, (a) because of coadaptation of (upstream) chirality genes and (downstream) modifiers (Diver and Andersson-Kottö [1938]; Gould et al. [1985]), and (b) because of reproductive incompatibility problems, particularly in species with globose shells (Asami, et al., 1998). So, most speciation events do not involve a reversal of chirality. But a small proportion (perhaps around 1%) do, and in these cases the switch is followed by re-coadaptation of modifiers and an entrenchment of the new chiral form. Thus, once switched, there is a tendency not to switch back again, with a few exceptions, notably Partula. Overall, then, there is no trend from dextrality to sinistrality (or vice versa), but rather large clades characterized by one form or the other, sometimes with large-ish subclades of the complementary type.
Intraspecific variation
Most gastropod species are fixed for one coiling direction or the other, except for the very occasional occurrence of the "wrong" form (Pelseneer, 1920; Robertson, 1993), these aberrant individuals being equivalent, in a sense, to the rare occurrence of left–right reversed ("situs inversus") humans. However, three species are known in which at least some natural populations are polymorphic for the direction of coiling: see Table 3.
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The formal genetics of chirality, as summarized in the table, were established through the work of Boycott and Diver (1923)
, Sturtevant (1923), Degner (1952) and Murray and Clarke (1966). The actual genes involved are not yet known, though given the long–range homologies of many developmental genes, it is tempting to speculate that homologues of some of the many known vertebrate left–right asymmetry genes are involved (see Rodriguez Esteban et al. (1999) and references therein). As in the case of centipedes, we can readily envisage an allopatric speciation scenario, where an isolated population of a normally dextral species becomes sinistral (though why this should happen, given the reproductive problems, remains unclear), and ultimately, having accumulated various other divergent properties, becomes a new species. And in this case, the "Atlanta law" does not come into play in that any one switch in chirality is as "major" as another. However, this "law" may simply apply at a higher level. For example, chirality switches are not particularly informative about how the unique gastropod body plan in which chirality is manifested arose in the first place.
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DISCUSSION |
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We now return to the question posed at the outset: do major evolutionary changes in adult phenotype arise from early developmental re-programming? The examples discussed above suggest that the answer to this question may be "usually but not always," as proposed in the cone model (Arthur, 1997
).
We will consider gastropod chirality first this time as the situation is simpler there. Gastropod development starts with the process of spiral cleavage, the first three steps of which result in the production of 2, 4 then 8 cells. The "handedness" of the adult is determined at least as early as the 8-cell stage, and possibly earlier (Verdonk and Van den Biggelaar, 1983). So in this case, the "developmental re-programming" (Arthur, 2000) is about as early as it possibly can be.
The situation regarding centipede segments is less straightforward. In geophilomorphs and scolopendromorphs, development is "epimorphic," meaning that all segments are laid down in the egg, so that the tiny hatchling already has its complete adult complement of segments. Studies on dechorionated eggs have shown that segmental anlagen are apparent quite early in embryonic development (Heymons, 1901), though of course considerably after the end of the cleavage stage. So for these two taxa, the developmental re-programming is again early, though less so than in the case of gastropod chirality.
Lithobiomorphs, scutigeromorphs and craterostigmomorphs, in contrast, develop anamorphically—that is, they continue to add segments at the posterior end during post-embryonic development, ending up with the adult complement of 15 only at the final pre-adult moult. Of course, the number of segments may be determined much earlier than the segments actually appear.
The evolutionary divergence that led to the Epimorpha (Scolopendromorpha + Geophilomorpha) thus involved two crucial changes: the addition of 8 (or 6) segments (Fig. 1); and the shift from anamorphic to epimorphic development. The fact that this latter shift occurred makes the former change (the increase in segment number) impossible to classify as "early" or "late" re-programming. Rather, what we have here is a heterochronic change (a sub-category of re-programming: Arthur, 2000), where overt segmentation is evolutionarily shifted into earlier ontogeny.
I would like to end on a broader note, namely the relationship of "evo-devo" with (a) neo-Darwinism and (b) cladistics. In one sense, it is perfectly compatible with both. It only makes sense to investigate the evolution of developmental changes against the background of a well-established (=molecular?) phylogeny. Also, most practitioners of evo-devo would agree that the major population-level force driving evolutionary alterations to ontogeny is natural selection, albeit this needs to include internal, as well as external, selective agents (Whyte, 1965; Arthur, 1997) or, to put it another way, both adaptation and coadaptation. However, there is a difference in emphasis between evo-devo and its longer-established partners relating to the heterogeneity of sizes and types of evolutionary change. Neo-Darwinism still owes much to Fisher's (1930) extreme micromutationist/gradualist view (see Orr, 1998), so evolution appears somewhat homogeneous from this perspective. And cladistics reinforces this homogeneous picture, if only because of its homogeneity of method, regardless of whether a genus-size or phylum-size clade is at stake. In contrast, heterogeneity of size, type and timing of evolutionary changes in development are at the heart of evo-devo. The patterns that surely lurk in this as-yet understudied heterogeneity are major targets for our research endeavour over the next few decades.
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ACKNOWLEDGMENTS |
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I thank Alec Panchen for his helpful comments on the manuscript.
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FOOTNOTES |
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1 From the Symposium Evolutionary Developmental Biology: Paradigms, Problems, and Prospects presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 4–8 January 2000, at Atlanta, Georgia.
2 E-mail: wallace.arthur{at}sunderland.ac.uk
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References |
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