How does segmentation help arthropods

However, there is no indication of an initial double-segment periodicity during sequential segmentation in the spiders Cupiennius Davis et al. This suggests that the ancestral arthropod segmentation clock had a single-segment periodicity, and that pair-rule patterning in insects and centipedes originated independently.

Beyond this, it is not clear exactly when or how many times pair-rule patterning evolved in either of the centipede or insect lineages. However, the dynamics of the Lithobius segmentation clock will need be investigated to rule out a transient or cryptic double-segment periodicity. In insects, most of the available data come from holometabolan or orthopteran species, as well as the cockroach Periplaneta and the hemipteran bug Oncopeltus Fig.

Holometabolans Binner and Sander, ; Nakao, ; Patel et al. Consistent with this possibility, gene expression in Periplaneta more closely related to orthopterans than to holometabolans appears to be single-segmental Pueyo et al.

Thus, although the evidence from some of these species is ambiguous, the current picture suggests that pair-rule patterning may have evolved within crown-group insects, possibly multiple times. This is puzzling, because the specialised and relatively invariant body plan of insects presents a morphological constraint that is hard to reconcile with a saltational doubling of segmentation rate. Given that Strigamia seems to switch to a single-segment periodicity when adding its most posterior segments Brena and Akam, , and that pair-rule patterns are seen during the anterior patterning of otherwise segmental species Dearden et al.

As pair-rule patterning requires half the number of clock cycles to generate a given number of segment-polarity stripes, its evolution may have been driven by selection for faster development in holometabolans or a longer body in centipedes.

However, it is currently not obvious how the ancestral segment-patterning mechanism was modified to become pair-rule. Alternatively, the clock itself could have been modified, e. To reconstruct the specific regulatory changes that occurred, it will be informative to find out how the gene expression and enhancer logic of pair-rule species compares with their closest segmental relatives.

In arthropods, segment number is determined by the total number of pair-rule stripes and the periodicity with which they regulate segment-polarity genes. In simultaneously segmenting insects, such as Drosophila , individual pair-rule stripes are positioned by gap factors at specific locations along the AP axis, hardcoding segment number. In sequentially segmenting species, segment number instead depends on the temporal duration of segmentation, divided by the period of the segmentation clock.

Gap genes appear to play some role in controlling the duration of segment addition Cerny et al. Over time, gap genes are expressed sequentially within the SAZ, their turnover driven by cross-regulatory interactions Boos et al.

It evidently exerts some control over the body plan, as perturbing hunchback expression can both decrease Liu and Kaufman, ; Marques-Souza et al. These phenotypes are not well understood, but might result from gap genes directly or indirectly regulating cell behaviour within the SAZ.

Such effects are unlikely to be mediated via the Hox genes, because significant perturbations of Hox gene expression in insects and crustaceans have not been found to affect segment number Angelini et al.

Despite varying widely among arthropods, segment number is usually fixed within a species. However, there are certain groups, such as geophilomorph centipedes, in which naturally occurring variation might provide clues as to how this number evolves Kettle and Arthur, ; Vedel et al. Another interesting question is how species that undergo post-embryonic segmentation coordinate segment patterning with the moult cycle.

Ecdysone-related genes play segmentation roles in some embryos Erezyilmaz et al. These elements receive spatial information from gap factors, and each drives expression at a different AP position or pair of positions along the blastoderm, contributing just one or two stripes to a gene's overall 7-stripe pattern.

Sepsid flies which diverged from drosophilids about million years ago are also known to use this kind of element Hare et al. Simultaneous segmentation, typified by Drosophila , is traditionally thought of as mechanistically distinct from sequential segmentation, typified by, for example, Tribolium or Gryllus. However, the Drosophila blastoderm is now known to be more dynamic than was previously imagined, and the basic structure of its segment patterning network seems remarkably similar to that of other arthropods Fig.

Reconciling sequential and simultaneous segmentation. A Structural overview of arthropod segmentation gene networks. The core of the system yellow box is relatively conserved across species.

In sequential segmentation, spatial information is provided by the timing factor network, which generates a wavefront. Gap genes do not play a major role in segment patterning, although late gap gene expression may be important for terminating segmentation, by repressing timing factors that maintain the SAZ dashed blue line. In simultaneous segmentation, timing factors only provide temporal information.

Spatial information is usually provided by a novel anterior patterning centre i. Gap genes pass this information to the primary pair-rule genes, through newly evolved regulatory elements SSEs. B Spatial patterning in Drosophila is inherently dynamic. Note that each panel zooms in on a smaller region of the AP axis. C Schematic kymographs i. In sequential segmentation, timing factor expression blue matures from anterior to posterior across the tissue, producing a wavefront diagonal line.

Periodicity is generated by sustained oscillations note how even skipped turns on and off over time within the blue zone. The wavefront converts the oscillations into a stable segment-polarity pattern engrailed expression.

In simultaneous segmentation, there is little spatial regulation of timing factor expression across the tissue, and pair-rule stripes are present from the start.

Embryo diagrams depict the specific time points they line up with on the kymographs eve expression is not shown. Patterning has double-segment periodicity. Note that the two time axes have different scales. As the Drosophila blastoderm stage is so short, the effects of dynamic gene expression are subtle, and for years were overlooked.

However, quantitative expression atlases suggest that expression domains in the posterior half of the blastoderm travel anteriorly across cells over time Jaeger et al. The shifts reflect sequential patterns of transcriptional states within cells, and trace back to asymmetric repressive interactions in the gap gene network Jaeger, ; Verd et al.

In the Drosophila blastoderm, the expression dynamics of the gap genes are directly transferred to pair-rule genes via their SSEs Fig. Some primary pair-rule genes, and both secondary pair-rule genes, possess zebra elements. These regulatory interactions are also dynamic, and they combine with the stripe shifts driven by the gap genes to generate a staggered sequence of pair-rule gene expression within each double-segment repeat Clark, Fig. This spatiotemporal sequence is the same as that driven by the segmentation clock in sequentially segmenting species such as Tribolium and Strigamia Choe et al.

Once primary pair-rule gene expression is properly phased within each double-segment repeat, Drosophila segment patterning proceeds just as it would in the anterior SAZ of a sequentially segmenting species, beginning with the activation of prd and slp , and moving on to segment-polarity gene expression and stripe doubling. This conserved process of pattern resolution is apparently regulated by a conserved sequence of timing factor expression: posterior SAZ factors Caudal and Dichaete are expressed throughout the trunk during the early, dynamic stages of pair-rule gene expression in Drosophila , and are replaced by the anterior SAZ factor Opa as the segment-polarity pattern is being resolved Clark and Peel, The Drosophila blastoderm therefore seems effectively equivalent to a SAZ, except that rather than maturing gradually from anterior to posterior, it does so all at once Fig.

We suspect that much of the ancestral segmentation machinery remains intact. However, as spatial information is no longer conveyed by the delayed maturation of posterior tissue, gap genes and SSEs preload it into the system instead Fig. Importantly, although genetic perturbations tend to result in different phenotypes in the two modes of segmentation e.

Simultaneous segmentation differs from sequential segmentation in two key respects: its temporal regulation determined by the expression profiles of the timing factors , and the spatial pre-patterning of the pair-rule genes by gap genes Fig. Simultaneous segmentation is also associated with an anterior shift of the blastoderm fate map and an increase in the number of segments patterned prior to gastrulation.

The evolution of simultaneous segmentation appears to be constrained by early embryogenesis French, These species pattern their segments sequentially. These species frequently have a biphasic mode of segmentation, in which anterior segments are patterned simultaneously.

Meroistic ovaries which facilitate pre-patterning of the egg , may therefore be a pre-adaptation for simultaneous segmentation. Extreme examples of simultaneous segmentation e.

Drosophila have evolved independently within each of the major holometabolan orders Davis and Patel, A Drosophila -like mode of segmentation likely requires far-reaching changes to early embryogenesis, such as a novel anterior patterning centre to help spatially pattern gap genes along the entire AP axis of the egg Lynch et al.

Here, we focus on understanding how SSEs and gap genes are together able to take over stripe patterning from the clock.

It seems likely that this transition to intricate spatial regulation involves a series of selectively favourable regulatory changes, which incrementally increase the speed or robustness of segmentation, while strictly preserving its output Fig. The evolution of simultaneous segmentation involves a gradual replacement of the segmentation clock by SSEs.

A Clock enhancers potentially homologous to zebra elements and SSEs both drive stripes that shift anteriorly over time. SSEs can therefore gradually assume regulatory control over particular clock-driven stripes i-iv , without disrupting downstream patterning. B Simultaneous patterning is likely to evolve stepwise along the AP axis, via the acquisition over evolutionary time of new SSEs that control expression in increasingly posterior stripes.

Embryo diagrams assume a segmentation clock with double-segment periodicity. In addition, simultaneous patterning is likely to evolve stepwise within each pair-rule gene expression repeat, as more of the primary pair-rule genes evolve their own SSEs. Additional SSEs reduce the time required to organise pair-rule gene expression across the repeat. As a consequence, the magnitude of the stripe shifts can decrease.

C Changes in gap gene expression can be sufficient to generate additional SSE-driven stripes, without accompanying changes in cis-regulatory logic. The current situation likely evolved from a simpler scenario left , in which the same enhancers drive expression in only one stripe each. Diagrams are colour-coded such that transcription factor names top have the same colour as their corresponding expression domain s below.

First, new SSEs seem to be easy to evolve, because they tend to be short, with simple regulatory logic and high sequence turnover between closely related species Hare et al. Some of them may have been selected simply to increase the robustness of segmentation clock expression; this might have occurred in either a blastoderm or a SAZ context.

Second, only a single new SSE need evolve at one time. Simultaneous patterning seems likely to have evolved progressively, from anterior to posterior, with each new SSE-driven stripe reducing the number of cycles needed from the clock Peel and Akam, Fig. Furthermore, cross-regulation between the pair-rule genes means that an SSE for one gene could in principle go on to organise a whole pattern repeat, with the remaining genes evolving their own SSEs afterwards, to make patterning faster or more robust Clark, Fig.

This process might be highly contingent: in Drosophila , eve and runt have full sets of SSEs and odd is patterned largely through cross-regulation Schroeder et al. Finally, SSEs can be reused. In Drosophila there are several SSEs that drive a pair of stripes, typically arranged symmetrically around a particular gap domain Schroeder et al. This suggests that posterior gap gene expression evolved to duplicate the regulatory environments of anterior stripes, thereby initialising additional pair-rule gene stripes without the need to evolve additional SSEs Fig.

Interestingly, Drosophila eve stripes 3 and 7, which are co-driven by a single SSE, are regulated by the same gap genes as are eve stripes 3 and 6 in Anopheles Goltsev et al. This hypothesis is hard to reconcile with the gradualist scenario we favour, as the transitional states would have severely compromised fitness. In support of this alternative, a midge species more closely related to Drosophila than to Anopheles patterns only five eve stripes before gastrulation Rohr et al. Our current understanding is that arthropod segment patterning is an inherently dynamic and a significantly conserved process, ancestrally taking the form of a clock-and-wavefront system.

Note, however, that many of the conclusions in this Review extrapolate from fragmentary data gathered from a small number of model species, with functional data available from an even smaller number.

This is certainly not the last word on arthropod segmentation, but we hope to have provided a coherent framework for further thought and experiment. We anticipate that future investigation will centre on two contrasting but inter-related tasks. First, better resolving the nature of the ancestral arthropod clock-and-wavefront system: the topology of the gene regulatory networks comprising the clock, the production of timing factor wavefronts by a retracting SAZ, and the mechanistic basis for the interactions between them.

Second, reconstructing how arthropod segmentation networks have diversified over time, giving rise to such remarkable novelties as simultaneous patterning and double-segment periodicity. In addition, we believe that sequentially segmenting arthropod models are well placed to complement and inform the study of vertebrate axial patterning, especially given their benefits of cost-efficiency, short generation times, experimental tractability, and relatively simple genomes.

The most pressing next step is to collect good-quality multiplexed expression data from a variety of arthropod species Choi et al. Building on a solid descriptive foundation, there are numerous exciting directions to pursue: genome editing to generate mutants, misexpression constructs, and live reporters Gilles et al. Over the past four decades, arthropod segmentation has contributed enormously to our understanding of developmental gene networks and their evolution.

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Find out more about the Node Network. Sign In or Create an Account. Advanced Search. User Tools. Sign in. Skip Nav Destination Article Navigation. Close mobile search navigation Article navigation. Volume , Issue Previous Article Next Article. Article contents. Nature of the arthropod segmentation clock. Segment patterning by the pair-rule network.

The evolution of simultaneous segmentation. Article Navigation. Arthropod segmentation Erik Clark X. This site. Google Scholar. Andrew D. Peel Michael Akam Michael Akam. Author and article information. Competing interests The authors declare no competing or financial interests. Online Issn: Published by The Company of Biologists Ltd. Development 18 : dev Cite Icon Cite. View large Download slide. Box 1. The evolutionary origins of arthropod segmentation. Box 2. Regulation of segment number.

Embryology and Phylogeny in Annelids and Arthropods. Search ADS. Functional analyses in the milkweed bug Oncopeltus fasciatus Hemiptera support a role for Wnt signaling in body segmentation but not appendage development. Hox gene function and interaction in the milkweed bug Oncopeltus fasciatus Hemiptera. Growth zone segmentation in the milkweed bug Oncopeltus fasciatus sheds light on the evolution of insect segmentation.

Dynamics of growth zone patterning in the milkweed bug Oncopeltus fasciatus. A context-dependent combination of Wnt receptors controls axis elongation and leg development in a short germ insect. A revised understanding of Tribolium morphogenesis further reconciles short and long germ development. Pair-rule patterning in the honeybee Apis mellifera: expression of even-skipped combines traits known from beetles and fruitfly. Multiple Wnt genes are required for segmentation in the short-germ embryo of Tribolium castaneum.

The concept of segmentation in biology relies upon the ability for organisms to duplicate organs and structural elements, such as arms and legs. Segmentation allows for more variety among species. In biology, the segmentation follows the longitudinal axis the length of the body from head to tail and separates the different body functions into separate systems such as the circulatory, digestive, nervous and excretory systems.

Each segment plays a significant role that relies upon other functions to work. For example, humans consist of heteromeric segmentation, in which each segment differs from another and fulfills a specific role. Homomeric segmentation refers to segments that contain similar elements, such as with the segments in an Errantia, a type of worm. Annelids The first segmented animals to evolve were the annelid worms, phylum Annelida.

These advanced coelomates are assembled as a chain of nearly identical segments, like the boxcars of a train. The great advantage of such segmentation is the evolutionary flexibility it offers—a small change in an existing segment can produce a new kind of segment with a different function. Thus, some segments are modified for reproduction, some for feeding, and others for eliminating wastes.

Two-thirds of all annelids live in the sea about 8, species, including the bristle; most of the rest—some 3, species—are earthworms. The basic body plan of an annelid is a tube within a tube: The digestive tract, is suspended within the coelom, which is itself a tube running from mouth to anus. There are three characteristics of annelid body organization: Repeated segments. The body segments of an annelid are visible as a series of ringlike structures running the length of the body, looking like a stack of doughnuts.

In each of the cylindrical segments, the excretory and locomotor organs are repeated. The body fluid within the coelom of each segment creates a hydrostatic liquid-supported skeleton that gives the segment rigidity, like an inflated balloon. Muscles within each segment pull against the fluid in the coelom. Because each segment is separate, each can expand or contract independently. When an earthworm crawls on a flat surface, for example, it lengthens some parts of its body while shortening others.

Specialized segments. The anterior front segments of annelids contain the sensory organs of the worm. Elaborate eyes with lenses and retinas have evolved in some annelids. One anterior segment contains a well-developed cerebral ganglion, or brain.

This characteristic, which researchers call segmentation, is shared by three large groups of animals. It may not be obvious at first glance though, as the repeated segments can be hidden by a shell or be partially fused.

The segments are nevertheless present, laid out along the bilateral axis in the trunk, abdomen or thorax. The first of these animal groups is the arthropods, which include centipedes but also insects, spiders, scorpions and crustaceans, representing by far the largest group of animals on the planet.

Apart from centipedes, whose segmentation is impossible to miss, arthropods also include grasshoppers, crickets and shrimps. Vertebrates, another highly diverse group, come next. They comprise most familiar animals, including humans, and they represent an evolutionary success.

In this group, segmentation is found in the vertebrae of the backbone and, at a finer anatomical scale, in the muscles and nerves that spread from the spinal cord. The final group is the annelid worms, whose body is almost entirely formed of identical segments, such as sea and earthworms.

They are also very numerous in terms of species, though much less conspicuous. These three groups are not closely related to one another. So, where does their segmentation come from? Is it possible that they all inherited this feature from a very distant common ancestor that lived million years ago, before the Cambrian explosion, which produced most of the large animal groups that exist today? Or has segmentation occurred several times during the history of evolution?

The researchers found that the genes controlling segment formation during embryo development are almost the same in drosophila an arthropod and in annelid marine worms, on which they concentrated their studies.