The development and evolution of arthropod tagmata

Abstract

The segmented body is a hallmark of the arthropod body plan. Morphological segments are formed during embryogenesis, through a complex procedure involving the activation of a series of gene regulatory networks. The segments of the arthropod body are organized into functional units known as tagmata, and these tagmata are different among the arthropod classes (e.g. head, thorax and abdomen in insects). Based on embryological work on segment generation in a number of arthropod species, coupled with a survey of classical descriptions of arthropod development, I suggest a new framework for the evolution of arthropod tagmata. The ancestral condition involves three developmental tagmata: the pre-gnathal segments, a tagma that is formed within a pre-existing developmental field and a tagma that is formed through the activity of a segment-addition zone that may be embryonic or post-embryonic. These embryonic tagmata may fuse post-embryonically to generate more complex adult tagmata. This framework is consistent with the evolution of tagmosis seen in the early arthropod fossil record. It also calls for a re-thinking of the decades-old division of arthropod development into short-germ versus long-germ development, a re-thinking of questions of segment identity determination and the role of Hox genes in tagma differentiation.

Keywords: Hox genes; arthropods; body plan; segment identity; tagma.

Figure 1.

Schematic representation of the different modes of segment generation in four insect species. (a) In the milkweed bug Oncopeltus fasciatus, two of the pre-gnathal segments (red) and the gnatho-thoracic segments (green) are patterned nearly simultaneously in the blastoderm. Germ-band condensation (marked with a black arrowhead) occurs through a process of invagination. The abdominal segments (blue) are patterned sequentially in the germ band. The third pre-gnathal segment, the intercalary segment, is patterned during abdominal segmentation, as in many insects. (b) In the German cockroach Blattella germanica, there is no sharp distinction between a blastoderm and germ-band stage. However, the gnatho-thoracic segments are patterned rapidly and sequentially in a pre-patterned field, which then condenses to form the germ-band, where abdominal segmentation takes place. (c) In the well-studied fruit fly, Drosophila melanogaster, all segments are patterned simultaneously in the blastoderm, followed rapidly by the condensation of the germ-band. (d) In the flour beetle Tribolium castaneum, all segments are patterned sequentially. However, there is a difference in rate between the gnatho-thoracic segments and the abdominal segments, and the segment-addition zone is only active during abdominal segmentation. Germ-band condensation occurs simultaneously with gnatho-thoracic segmentation (marked with a broad black arrowhead).

Figure 2.

Schematic representation of the different modes of segmentation in four arthropod species. (a) In geophilomorph centipedes (such as Strigamia maritima), the germ band condenses (black arrowhead) during the segmentation of the pre-gnathal segments (red) and the gnathal segments (green), without the activity of a segment addition zone. Trunk segments (blue) are formed mostly two at a time (transparent fill and dotted lines indicate that not all segments are portrayed). Segmentation ends well before hatching (white arrowhead). (b) In scutigeromorph centipedes, anterior segmentation is probably similar to that of geophilomorph centipedes, although there is very little data). Four trunk segments form during embryogenesis, with successive segments added post-hatching. (c) In arachnids, including spiders and others, the pre-gnathal segments and the limb-bearing segments are patterned rapidly within the early embryonic disc. The disc then condenses to give the germ-band, and opisthosomal segments are patterned sequentially from a segment-addition zone. (d) In crustaceans that have a nauplius stage, the pre-gnathal segments and the mandibular segments are patterned embryonically. The germ-band condenses and the nauplius hatches, with additional segments added sequentially. In crustaceans without a nauplius stage (not shown), the main difference is that hatching is heterochronically shifted to after the end of segmentation.

Figure 3.

A schematic tree of the main panarthropod groups mentioned in the text, with the major evolutionary events related to tagmosis mapped on the tree. The tips are extant genera for which there exist developmental data. Genera listed vertically represent fossil species for which we have ontogenetic data. (a) In the common ancestor of Panarthropoda, there was a single-segment head and an undifferentiated trunk region. (b) Post-embryonic segment addition appeared in stem-group arthropods. This may also represent the first appearance of a segment addition zone. (c) Deuteropoda is characterized by the appearance of the three-segment head, representing a novel developmental tagma with a unique mode of segment generation: the pre-gnathal region. (d) The common ancestor of Arthropoda already had three distinct developmental tagmata: the pre-gnathal segments, a tagma including segments developing in a pre-existing field, and a tagma with segments generated from a segment addition zone. (e) Trilobites have a unique mode of tagmosis, involving segment release between the pygidium and the thorax. (f) All extant arachnids have a prosoma composed of the pre-gnathal segments and an embryonic tagma with four segments formed in a pre-existing field, and an opisthosoma, with a variable number of segments formed from a segment addition zone. In stem arachnids, the number of segments formed in each tagma varies, but the general arrangement is the same as in extant arachnids. (g) In myriapods, the number of segments formed within a pre-existing field is three or four, including the gnathal segments and possibly one post-gnathal segment. (h) The nauplius appeared early in the evolution of Pancrustacea, although it is not clear if it is a synapomorphy of the entire clade. All pancrustaceans have a pre-gnathal region and a tagma including segments generated from a growth zone. The number of segments developing within a pre-existing field is variable and may be as low as a single segment in some lineages. (i) In Malacostraca, the segment addition zone functions via specialized stem cells: ectoteloblasts. (j) In insects, the thorax, a novel tagma, first appears. It is composed of three of the segments formed within a pre-existing field, with an additional three segments, the gnathal segments, fusing with the head as in other mandibulates. (k) In Holometabola, the developmental distinction between gnatho-thoracic segments and abdominal segments is masked, with the evolution of novel segmentation modes.