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PalAss Home > PalAss Newsletter > Modularity in Palaeontology Subunit 2: Examples
Modularity in Palaeontology Subunit 2: Examples


In our last column (subunit 1), we outlined modularity, a concept used by evolutionary developmental biologists. The two columns were designed to spark interest amongst palaeontologists in the concept of modularity and to make us all think about our research areas from a different angle.

To recall, modules as independent yet interactive units of development and/or evolution may be structural, developmental, physiological or behavioural. New modules evolve by one of three processes – dissociation (a new function is taken on), duplication and divergence (new function taken on by the duplicate), or co-option (new modules incorporate functions from other modules) (see Subunit 1).

In this column we present some examples of how the concept of modularity is being used by palaeontologists, although not always recognized and cited as such. Our examples include mammalian inner ear ossicles, body patterning in trilobites, teeth, and appendages.

Ear ossicles: It has long been agreed amongst palaeontologists that elements composing the reptilian jaw joint (viz., the quadrate and articular) are homologous with the incus and malleus (both first arch derivatives), respectively of the mammalian middle ear. Supporting evidence comes from various independent sources, including the fossil record, embryology and developmental genetics. The fossil record shows us a virtually complete series beginning with the reptilian lower jaw, passing through various ‘intermediate’ stages of non-mammalian synapsids (in which there is an increase in dominance of the dentary and a reduction in the postdentary elements) and ending with the modern mammalian condition. Developmentally, the reptilian articular bone and a large portion of the mammalian malleus can be seen to form by ossification of one end of Meckel’s cartilage; the middle portion of Meckel’s, the embryonic cartilage of the lower jaw, then atrophies leaving the incus and malleus (and ectotympanic) attached to the ear region of the skull. Some of these transitional stages are visible in the embryogenesis of extant marsupials. More recently, it has been argued that developmental genetics has shown that gene knock-outs can reveal ancestral patterns in the mutant phenotype (although see Smith and Schneider [1998] for an alternative interpretation). This is a classic and remarkable example of evolutionary transformation.

The middle ear ossicles lie at the junction of the first and second branchial arch, which is an evolutionarily important region. One can consider the elements of the reptilian lower jaw as entities or modules that can evolve (into ear ossicles), which undergo dissociation (assuming a new function in mammals) and which shift in space (migrating to the middle ear in mammals). Evidence that this module can also evolve independently comes from a recent description of the dentary of the oldest known monotreme, the Early Cretaceous Teinolophos, in which Rich et al. (2005) show that the mammalian middle ear evolved independently in living monotremes and therians (marsupials and placentals) at least twice. This module is under the control of master developmental genes, the Hox genes. Knocking out Hox genes in mouse embryos results in malformations of this region, specifically the duplication of elements, which are often regarded as resurrected reptilian bones. For a further discussion of the evolution of the lower jaw elements in reptiles and the middle ear ossicles in mammals, and more discussion on the molecular regulation of these elements, see Box 13.1 in Hall (2005 and references therein).

Trilobites: Nigel Hughes of the University of California published an insightful paper on body patterning in trilobites (Hughes, 2003), which exemplifies how the concept of modularity illuminates the evolution of tagmosis in arthropods. Tagmosis is the process by which an animal body is subdivided into tagma (segments), which, either individually or as groups, exhibit structural and functional distinctness and can thus be considered modules. Ten thousand species of trilobites extending over a 270 Myr history is an astonishing database for such analyses. By coupling an analysis of tagmosis in trilobites with work on Hox gene expression in modern arthropods, Nigel was able to infer how Hox genes may have been employed in trilobites. He concentrates on the trunk region, demonstrating that several derived clades of trilobites independently evolved functionally-distinct trunk tagmata, based on what Hughes calls “two-batch” trunk regionalization. He makes the case that trilobites ‘took advantage of’ the flexibility of segment numbers in the trunk – a flexibility that is manifest both in ontogeny and over phylogenetic lineages – that allowed evolution of independence of regions within the trunk; much as gene duplication provides the flexibility to free up a gene(s) for a new function. This is another example of modular dissociation. His approach illustrates the lack of congruence between boundaries of Hox gene expression in modern arthropods and the morphology of the same animals; and how our emphasis on segments with different morphologies (rather than numbers) and groupings of segments without boundaries that define between segment classes, has limited our ability to link body form with developmental control. As Hughes notes in concluding his paper: “Cases such as trilobite trunk evolution…, in which fossils provide the empirical record of the development of a major evolutionary innovation, demonstrate palaeontology’s unique and integral role within evolutionary developmental biology” (p. 395).

Teeth: A third example of modularity. The fundamental unit from which teeth and early vertebrate scales arose is the odontode. The basic odontode consists of three subunits – a dentine cone with internal pulp cavity, a base of laminar bone and a cap of hypermineralized tissue (viz., enamel). These three modules are often considered as one fundamental unit of tooth development. However, each module can interact during developmental, and can be separated over the course of evolution. Delving into the fossil record reveals many examples of animals that do not have all three subunits of the basic odontode. For example, galeaspid scales only have two modules – the base of laminar bone and the enamaloid cap; some heterostracans (psammosteid) have the basal bone and the dentine-covered cones but lack any hypermineralized tissue. As revealed by the fossil record, the three tissues in each module of the basic tooth (skeletal base, dentine, and enamel) have evolved in different ways and at different rates. These subunits can therefore be viewed as three separable evolutionary modules, a notion introduced by White (2004).,br>
Appendages: Through time, appendages of invertebrates and vertebrates have been modified as feeding, locomotory, reproductive and sensory structures. The multiple functions didn’t necessarily evolve in any order but are commonly found within one individual. Lobsters, for example, have podia modified for feeding, reproduction, defence and locomotion. It could be argued that the appendage developmental module is the most labile module considering the astounding diversity of appendage structures and functions that arose from a similar developmental module. The evolutionary flexibility of the appendage module was apparent early on in life history; the Cambrian was replete with invertebrates exhibiting many sets of paired appendages that were used for different functions. The Burgess Shale fauna is rich with creatures with many types of appendage structures undoubtedly tailored for different functions.

The diversity of animal appendage structures is due largely to the modification of the expression of the gene package (appendage developmental module) responsible for patterning the appendages (Shubin et al., 1997). These authors comment how the paired appendages of vertebrates and invertebrates cannot be considered homologous as they do not share a common ancestor with paired appendages; they also develop completely differently (limb buds versus imaginal discs). However, by applying the concept of modularity to appendages we are provided with a meaningful way with which to compare serially homologous structures and those that arise through convergent evolution. We can compare the evolutionary histories of appendages in diverse groups because they have a developmental module in common. Given the astonishing diversity of appendages, it is perhaps not surprising that their evolution appears to have progressed through all three of the evolutionary processes modules can follow, namely dissociation (fins evolved into limbs with a reduction of the distal-most portion of the module), duplication and divergence (the duplication of the appendage developmental module facilitated the evolution of distinct locomotory and feeding appendages in arthropods), and co-option (some suggest that the origin of vertebrate fins is due to the co-option of the gut patterning genes into the paraxial mesoderm to form the appendage developmental module [Coates and Cohn, 1998]).

Different parts of vertebrate limbs (stylopodium, zeugopodium and autopodium) are structural modules arising from the developmental appendage module. We can discuss the evolution of the autopodium, for example, distinct from the developmental appendage module, knowing that the variability in autopodium structures in vertebrates is due to the modifications of the appendage developmental module. The compliment of genes involved in the development of the autopodal structures can also be considered a developmental module. In other words the autopodium is a structural module that has a structure determined by the appendage developmental module and the autopodium developmental module.

Vertebrate limbs are a fantastic biologic system to which the concept of modularity is applicable. Palaeontologists can use the concept of modularity in their studies of highly modified limbs that are only found in the fossil record, e.g., most agnathans, plesiosaurs, ichthyosaurs, mosasaurs, etc. The concept of modularity provides evolutionary biologists, including palaeontologists, a construct in which to examine evolutionary process from evolutionary pattern.

We hope to have inspired you to use the concept of modularity in your studies and that modularity will be referenced more in the palaeo-literature in the near future.


REFERENCES
COATES M.I. and COHN M.J. 1998. Fins, limbs, and tails: outgrowths of and axial patterning in vertebrate evolution. BioEssays 20: 371–381.

HUGHES N. 2003. Trilobite body patterning and the evolution of arthropod tagmosis. BioEssays 25:4: 386–395.

HALL B.K. 2005. Bones and Cartilage. Developmental and Evolutionary Skeletal Biology. London: Elsevier/Academic Press.

RICH T.H., HOPSON J.A., MUSSER A.M., FLANNERY T.F., and VICKERS-RICH P. 2005. Independent origins of middle ear bones in monotremes and therians. Science 307: 910–914.

SHUBIN N., TABIN C. and CARROLL S. 1997. Fossils, genes and the evolution of animal limbs. Nature 388: 639–647.

SMITH K.K. and SCHNEIDER R.A. 1998. Have gene knockouts caused evolutionary reversals in the mammalian first arch? BioEssays 20: 245–255.

WHITE A.T. 2004. Teeth: Overview. Palaeos website (accessed: February 2006).




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