Ariel D. Chipman

Arthropod Segmentation: beyond the Drosophila paradigm

Most of our knowledge about the mechanisms of segmentation in arthropods comes from work on Drosophila melanogaster. In recent years it has become clear that this mechanism is far from universal, and different arthropod groups have distinct modes of segmentation that operate through divergent genetic mechanisms. We review recent data from a range of arthropods, identifying which features of the D. melanogaster segmentation cascade are present in the different groups, and discuss the evolutionary implications of their conserved and divergent aspects. A model is emerging, although slowly, for the way that arthropod segmentation mechanisms have evolved.

The segmentation cascade in the centipede Strigamia maritima: Involvement of the Notch pathway and pair-rule gene homologues

The centipede Strigamia maritima forms all of its segments during embryogenesis. Trunk segments form sequentially from an apparently undifferentiated disk of cells at the posterior of the germ band. We have previously described periodic patterns of gene expression in this posterior disc that precede overt differentiation of segments, and suggested that a segmentation oscillator may be operating in the posterior disc. We now show that genes of the Notch signalling pathway, including the ligand Delta, and homologues of the Drosophila pair-rule genes even-skipped and hairy, show periodic expression in the posterior disc, consistent with their involvement in, or regulation by, such an oscillator. These genes are expressed in a pattern of apparently expanding concentric rings around the proctodeum, which become stripes at the base of the germ band where segments are emerging. In this transition zone, these primary stripes define a double segment periodicity: segmental stripes of engrailed expression, which mark the posterior of each segment, arise at two different phases of the primary pattern. Delta and even-skipped are also activated in secondary stripes that intercalate between primary stripes in this region, further defining the single segment repeat. These data, together with observations that Notch mediated signalling is required for segment pattern formation in other arthropods, suggest that the ancestral arthropod segmentation cascade may have involved a segmentation oscillator that utilised Notch signalling.

Early development and segment formation in the centipede, Strigamia maritima (Geophilomorpha).

Summary Geophilomorph centipedes exhibit a number of unique characteristics that make them of particular developmental and evolutionary interest. Segment numbers in geophilomorphs are higher than in any other centipedes, ranging from 27 to 191. They may be constant within a species, presenting in extreme form the “counting” problem in development, or they may vary—a situation that provides us with the opportunity to study naturally occurring variation in segment numbers. All their segments are generated during embryogenesis, a situation unlike that in the more basal centipede orders, which generate only a fraction of their 15 trunk segments in the embryo and develop the rest postembryonically. Here we provide a foundation for further developmental studies of the Geophilomorpha, building on the one study that has been conducted to date, on the coastal species Strigamia maritima. Development begins with the migration of nuclei to the surface of the egg, which then condense to form an embryonic rudiment of more than 20,000 cells, covering an entire hemisphere. During early development, the embryo can be divided into two distinct areas: a large terminal disc of apparently undifferentiated tissue and the germ‐band, which has a clear anteroposterior axis and differentiated segments. The germ‐band forms from the anterior of the terminal disc and extends anteriorly as the disc contracts. New segments are formed at the posterior margin of the germ‐band. Once the process of segmentation ends, the germ‐band folds and sinks into the yolk. We note that the classic description of centipede development, by Heymons more than a century ago, contains a fundamental error in the identification of the axes and hence in the interpretation of early segmentation.

Parallel evolution of segmentation by co-option of ancestral gene regulatory networks

Different sources of data on the evolution of segmentation lead to very different conclusions. Molecular similarities in the developmental pathways generating a segmented body plan tend to suggest a segmented common ancestor for all bilaterally symmetrical animals. Data from paleontology and comparative morphology suggest that this is unlikely. A possible solution to this conundrum is that throughout evolution there was a parallel co‐option of gene regulatory networks that had conserved ancestral roles in determining body axes and in elongating the anterior‐posterior axis. Inherent properties in some of these networks made them easily recruitable for generating repeated patterns and for determining segmental boundaries. Phyla where this process happened are among the most successful in the animal kingdom, as the modular nature of the segmental body organization allowed them to diverge and radiate into a bewildering array of variations on a common theme.

Neurogenesis in myriapods and chelicerates and its importance for understanding arthropod relationships

Several alternative hypotheses on the relationships between the major arthropod groups are still being discussed. We reexamine here the chelicerate/myriapod relationship by comparing previously published morphological data on neurogenesis in the euarthropod groups and presenting data on an additional myriapod (Strigamia maritima). Although there are differences in the formation of neural precursors, most euarthropod species analyzed generate about 30 single neural precursors (insects/crustaceans) or precursor groups (chelicerates/myriapods) per hemisegment that are arranged in a regular pattern. The genetic network involved in recruitment and specification of neural precursors seems to be conserved among euarthropods. Furthermore, we show here that neural precursor identity seems to be achieved in a similar way. Besides these conserved features we found 2 characters that distinguish insects/crustaceans from myriapods/chelicerates. First, in insects and crustaceans the neuroectoderm gives rise to epidermal and neural cells, whereas in chelicerates and myriapods the central area of the neuroectoderm exclusively generates neural cells. Second, neural cells arise by stem-cell-like divisions of neuroblasts in insects and crustaceans, whereas groups of mainly postmitotic neural precursors are recruited for the neural fate in chelicerates and myriapods. We discuss whether these characteristics represent a sympleisiomorphy of myriapods and chelicerates that has been lost in the more derived Pancrustacea or whether these characteristics are a synapomorphy of myriapods and chelicerates, providing the first morphological support for the Myriochelata group.

Variation in anuran embryogenesis: Differences in sequence and timing of early developmental events

Comparative embryology of closely related species can shed light on the evolution of developmental processes. An important mechanism in the evolution of developmental processes, which can lead to significant changes in larval or adult form, is variation in the sequence and timing of developmental events. We compared the development of 12 species of anurans, including a wide taxonomic range as well as a number of congeneric species. The comparison consisted of monitoring a series of external morphological markers and histological markers. For each species we noted the timing of each of the markers, using a uniform parameter of normalized time. We compared the normalized time of each of these events among the species, as well as the sequence of the events. Our analysis revealed many differences in sequence and in timing of developmental events. We mapped these differences on a cladogram of the studied species, using sequence units as discrete characters. The differences do not seem to be connected to the phylogenetic relations between the species or to any obvious ecological factors. We suggest a hypothetical ancestral sequence of developmental events, and discuss the possible factors that could have caused the observed variations from the ancestral sequence.

Expression of trunk Hox genes in the centipede Strigamia maritima: sense and anti-sense transcripts

SUMMARY We report the coding sequence and embryonic expression of the four trunk Hox genes Antennapedia (Antp), Ultrabithorax (Ubx), abdominal‐A (abd‐A), and Abdominal‐B (Abd‐B) in the geophilomorph centipede Strigamia maritima. In geophilomorph centipedes, all leg‐bearing segments (LBS) are generated during embryogenesis, allowing us to define expression in relation to the full extent of the forming trunk. Persistent Antp expression characterizes the maxillipedal (poison claw) segment, whereas all LBS express the three Hox genes Antp, Ubx, and abd‐A. Abd‐B is never detectably expressed in segmented tissue, but is restricted to a zone around the proctodaeum that contributes to the hindgut. Expression of all these Hox genes initiates in the unsegmented tissue of the blastodisc, with expression of Antp respecting a sharply defined anterior border before the appearance of morphological segmentation in the trunk. The accumulation of Hox gene transcripts is strongly modulated by the maturing segment pattern, suggesting regulatory interactions with multiple levels of the segment patterning machinery. For one of these genes, Ubx, we detect both sense and anti‐sense transcripts. The anti‐sense transcripts originate 3′ to the Ubx coding sequence and overlap the homeobox exon; they are expressed earlier than the Ubx coding transcripts and persistently, in an axially restricted pattern comparable to but distinct from those of the Hox coding transcripts. The pattern of accumulation of Ubx sense and anti‐sense transcripts is strikingly complementary, suggesting the possibility of anti‐sense regulation of Ubx expression.

Variation, plasticity and modularity in anuran development

Although anuran development is generally thought to be relatively conservative, a great deal of variation is evident when different species are compared. This report summarizes the results of comparative analyses of different aspects of anuran development. These include differences in sequence and timing of developmental events, the effects of genome size, and the effects of different life history strategies on anuran embryogenesis. The results show that anuran development is plastic at the evolutionary level, and many changes can occur in the developmental processes of anurans throughout their evolution. Changes are apparently rapid, and are as common as cladogenic events. This evolutionary plasticity can be attributed to the modular nature of anuran development. Different modules can shift relative to one another in time or in space, creating variations in the observed developmental patterns. However, shifts in modules can occur even without having a significant effect on the ultimate outcome of the process. I discuss the implications of the modular nature of development on the evolution of anuran development, and of the group in general.

Temperature-dependent plasticity of segment number in an arthropod species: the centipede Strigamia maritima

SUMMARY The evolution of arthropod segment number provides us with a paradox, because, whereas there is more than 20‐fold variation in this character overall, most classes and orders of arthropods are composed of species that lack any variation in the number of segments. So, what is the origin of the higher‐level variation? The centipede order Geophilomorpha is unusual because, with the exception of one of its families, all species exhibit intraspecific variation in segment number. Hence it provides an opportunity to investigate how segment number may change in a microevolutionary context. Here, we show that segment number can be directly altered by an environmental factor (temperature)—this is the first such demonstration for any arthropod. The direction of the effect is such that higher temperature during embryogenesis produces more segments. This potentially explains an intraspecific cline in the species concerned, Strigamia maritima, but it does not explain how such a cline is translated into the parallel interspecific pattern of lower‐latitude species having more segments. Given the plastic nature of the intraspecific variation, its link with interspecific differences may lie in selection acting on developmental reaction norms.

Early patterning and blastodermal fate map of the head in the milkweed bug Oncopeltus fasciatus

The process of head development in insects utilizes a set of widely conserved genes, but this process and its evolution are not well understood. Recent data from Tribolium castaneum have provided a baseline for an understanding of insect head development. However, work on a wider range of insect species, including members of the hemimetabolous orders, is needed in order to draw general conclusions about the evolution of head differentiation and regionalization. We have cloned and studied the expression and function of a number of candidate genes for head development in the hemipteran Oncopeltus fasciatus. These include orthodenticle, empty spiracles, collier, cap ‘n’ collar, and crocodile. The expression patterns of these genes show a broad conservation relative to Tribolium, as well as differences from Drosophila indicating that Tribolium + Oncopeltus represent a more ancestral pattern. In addition, our data provide a blastodermal fate map for different head regions in later developmental stages and supply us with a “roadmap” for future studies on head development in this species.