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Developing an integrated understanding of the evolution of arthropod segmentation using fossils and evo-devo - PubMed

  • ️Tue Jan 01 2019

Developing an integrated understanding of the evolution of arthropod segmentation using fossils and evo-devo

Ariel D Chipman et al. Proc Biol Sci. 2019.

Abstract

Segmentation is fundamental to the arthropod body plan. Understanding the evolutionary steps by which arthropods became segmented is being transformed by the integration of data from evolutionary developmental biology (evo-devo), Cambrian fossils that allow the stepwise acquisition of segmental characters to be traced in the arthropod stem-group, and the incorporation of fossils into an increasingly well-supported phylogenetic framework for extant arthropods based on genomic-scale datasets. Both evo-devo and palaeontology make novel predictions about the evolution of segmentation that serve as testable hypotheses for the other, complementary data source. Fossils underpin such hypotheses as arthropodization originating in a frontal appendage and then being co-opted into other segments, and segmentation of the endodermal midgut in the arthropod stem-group. Insights from development, such as tagmatization being associated with different modes of segment generation in different body regions, and a distinct patterning of the anterior head segments, are complemented by palaeontological evidence for the pattern of tagmatization during ontogeny of exceptionally preserved fossils. Fossil and developmental data together provide evidence for a short head in stem-group arthropods and the mechanism of its formation and retention. Future breakthroughs are expected from identification of molecular signatures of developmental innovations within a phylogenetic framework, and from a focus on later developmental stages to identify the differentiation of repeated units of different systems within segmental precursors.

Keywords: Arthropoda; evo-devo; palaeontology.

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Conflict of interest statement

We declare no competing interests.

Figures

Figure 1.
Figure 1.

A scenario for the origin and evolution of arthropod segmentation (based on [4]). (a) A simple bilaterian with a short body; (b) extension of the anterior–posterior axis (A-P); (c) several organ systems become independently metameric and distributed along the A-P axis; (d) metamerism of the different systems becomes synchronized; (e) elements of all metameric systems are generated together from an undifferentiated segmental precursor. (Online version in colour.)

Figure 2.
Figure 2.

Phylogenetic relationships among key experimental model species of Panarthropoda and representative fossil taxa. Names of terminals at the top of the tree are extant genera of experimentally tractable model species. Names of terminals deep within the tree are fossil forms representing stem-groups of various extant taxa. Node names refer to crown-groups. Placement of some of the fossil taxa is still contentious (see text for examples).

Figure 3.
Figure 3.

Annulated (a) and arthropodized (b–e) frontal appendages (fa). (a) The ‘gilled lobopodian’ Kerygmachela kierkegaardi; (b–e) disarticulated Anomalocaris canadensis frontal appendages. Scales: (a–c) 10 mm, (d–e) 5 mm. (a) courtesy of J. Vinther; (b–e) courtesy of A. Daley (from [66]). (Online version in colour.)

Figure 4.
Figure 4.

Schematic of gap gene expression domains in limbs of onychophorans and in the different arthropod classes. The proximal side of the limb is to the left. Lighter colours represent lower expression levels or downregulation during development. Redrawn with a revised phylogeny from [70]. See source for references. (Online version in colour.)

Figure 5.
Figure 5.

Examples of anterior segmentation through ‘stripe-splitting’ in different arthropod taxa. (a,b) Blastoderm stages of the milkweed bug Oncopeltus fasciatus (Insecta). An anterior patch of wingless expression representing both the ocular (oc) and antennal (an) segment splits to give rise to two distinct expression domains. (c,d) Early development of the centipede Strigamia maritima (Myriapoda), showing the expression of hedgehog. The anterior expression stripe representing the ocular segment (blue arrow) splits first from a preliminary single stripe. This is followed by the separation of the antennal (green arrow) and intercalary (yellow arrow) segmental stripes. The expression stripe representing the mandibular segment (red arrow) appears independently. (e–g) Early germband embryo of the spider Parasteatoda tepidariorum (Chelicerata), showing expression of hedgehog (blue stain) and deformed (orange stain). The anterior expression of hedgehog starts as a single stripe, which splits once to give a stripe representing the pedipalpal segment (Pp) and a second stripe that soon splits again to give the stripes representing the ocular segment (Ce, cephalic lobe) and the cheliceral segment (Ch). Adapted (a,b) from [48], (c,d) from [93] and (e–g) from [94]. (Online version in colour.)

Figure 6.
Figure 6.

Segmental midgut diverticula (mgd) in Cambrian total-group Arthropoda. (a,b) The ‘gilled lobopodian’ Pambdelurion whittingtoni, scales 20 mm; (c) the isoxyid Isoxys acutangulus, scale 5 mm; (d) the megacheiran Leanchoilia superlata, scale 5 mm; (e,f) the trilobitomorph Kuamaia lata: left side of thorax, showing exopod flap (ef,) lamellar setae (ls) and diverticula on three segments, scales: (e) 2 mm and (f), 5 mm. (Online version in colour.)

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References

    1. Chipman AD, Erwin DH. 2017. The evolution of arthropod body plans: integrating phylogeny, fossils, and development—an introduction to the symposium. Integr. Comp. Biol. 57, 450–454. (10.1093/icb/icx094) - DOI - PubMed
    1. Edgecombe GD, Legg DA. 2013. The arthropod fossil record. In Arthropod biology and evolution (eds Minelli A, Boxshall G, Fusco G), pp. 393–415. Berlin, Germany: Springer.
    1. Chipman AD. 2010. Parallel evolution of segmentation by co-option of ancestral gene regulatory networks. Bioessays 32, 60–70. (10.1002/bies.200900130) - DOI - PubMed
    1. Chipman AD. 2019. Becoming segmented. In Perspectives on evolutionary developmental biology (ed. Fusco G.), pp. 235–244. Padova, Italy: Padova University Press.
    1. Shubin N, Tabin C, Carroll S. 1997. Fossils, genes and the evolution of animal limbs. Nature 388, 639–648. (10.1038/41710) - DOI - PubMed

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