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Maruzzo, Diego (2008) Morphogenesis and evolution of annuli in arthropod appendages. [Ph.D. thesis]

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Abstract (english)

A widely used distinction among articles that usually composed an arthropod appendage is the one between true articles and annuli. This distinction is often claimed to be based on the anatomy of the muscular system, true articles have intrinsic musculature while annuli do not. Annuli are also usually considered a subdivision of a true article. Recently, it has also been noted that annuli tend to be produced later during development. Observations on development of Drosophila appendages also seem to support a basic difference between the process that produce true article and the one that produce annuli.
In the present project I studied selected aspects of article anatomy and development, in order to understand: a) which are (if present) the developmental similarities among annuli of different appendages and different arthropods, and b) which are (if present) the developmental differences between annuli and true articles. I decided to focalise the research on two topics: a) the relationships between muscles, muscle insertions and joints, and b) the mechanism of annulation in flagellar structures (terminal part of an appendage composed of only annuli) and its relationship with growth at the cellular level. According to the definitions of true articles and annuli given above, the anatomy of the muscular system is the most important aspect. For the most studied true articles, those of insect leg, there is evidence of a close developmental relationship between the development of the arthrodial membrane cells (epidermal cells that produce the joint) and muscle insertions. However some variation is expected as annuli are supposed to be joint without any muscle insertion. Parts of appendages composed of only annuli often show indeterminate postembryonic increasing in the number of annuli. The mechanism by which new annuli are produced has been studied only in few species or groups, and only for the antennae. Where both the mechanism of article production and the overall growth have been studied, a close relationship between the two was noted, but little is known about the development of the epidermis (cellular division, differentiation and apoptosis) during segmentation.
Different models have been employed to study the relationships between muscles, muscle insertions and joints and these are: the naupliar appendages (first antennae and exopod of both second antennae and mandibles) of the cirriped crustacean Balanus improvisus Darwin, 1854, the exopod of the naupliar second antennae of the branchiopod crustacean Artemia sp., the antennae of the centipede Lithobius forficatus (Linnaeus, 1758) and the rami of the pleopods of the malacostracan crustacean Gammarus roeselii Gervais, 1835. In these models the segmentation, the muscular system and the postembryonic changes have been studied. Literature on naupliar appendages anatomy and postembryonic development has also been reviewed in detail.
There are some muscles running parallel to the proximo-distal axis throughout the first antennae and the exopod of both second antennae and mandibles in the nauplii of B. improvisus. These muscles have insertions on every joint. The exopod of both second antennae and mandibles increase in article number during naupliar development and new joints have new intermediate insertion of already present muscles. Very similar conditions are usually found in the naupliar appendages of other crustaceans.
Unexpected results have been obtained on the exopod of naupliar second antennae of Artemia. The exopod has 8-10 natatory setae (number with individual variation) on the posterior-ventral side, which have some cuticular folds at their base, resembling a joint; on the opposite side there are 8-14 (number with individual variation) cuticular folds. Number and position of setae and cuticular folds do not match and thus complete joints are lacking. Three muscles are present within the exopod; they run parallel to the proximo-distal axis and have insertions at the base of a seta (for the two muscles that are on that side) or on a cuticular fold (for the single muscle that run on that side). Since setae and cuticular folds do not match, there is mismatch also in the muscular insertions of the two sides.
In the antennae of L. forficatus there are four muscles that run parallel to the proximo-distal axis throughout their length. These muscles have an insertion on each joint. The rami of the pleopods of G. roeselii have two muscles that run parallel to the proximo-distal axis throughout their length, with insertion on each joint.
Thus, even if the articles of the antennae of Lithobius are usually considered true articles and those of the naupliar exopod of second antennae and mandibles of Balanus (and other crustaceans) as well as those of the rami of the pleopods of Gammarus are usually considered annuli, there is no difference on the presence/absence of muscular insertions. Anatomical differences are present in the structure of the muscular insertion (tendon matrix) and of the joint (extent of arthrodial membrane). All the appendages originally studied here or those discussed in the review that increase in article number during postembryonic development produce new joints with new intermediate insertions of already present muscles.
The mechanism of annulation in flagellar structures has been studied in detail in the flagellum of the second antennae of isopod crustaceans. Asellus aquaticus (Linnaeus, 1758) has been the main species studied, with observations on both normal postembryonic development and regeneration; other species studied have been Idotea chelipes (Pallas, 1766), Lirceus fontinalis Rafinesque-Schmaltz, 1820 e Sphaeroma serratum (Fabricius, 1787). Most of the flagellum of A. aquaticus is composed of "quartets": four articles units where each article has a specific setal distribution pattern. New articles and quartets are produced during the whole life, in the proximal part of the flagellum: the first article divides and produces articles that, relatively independently from each others, divides three more times producing a quartet. During regeneration the mechanism is identical, although there are some difference in the relative development of different quartets, irrespectively of the amputation point. In L. fontinalis (Asellidae) most of the flagellum is composed of couples of articles, each one of which bearing setae correspondent to those of two articles of an A. aquaticus quartet. The mechanism of production is also very similar, but articles produced by the first one divide just once. In L. fontinalis some variability is, anyhow, present and it is sometimes possible to observe three articles units (an article produced by the first one divided twice) and even four article units identical to those of A. aquaticus. In S. serratum (Sphaeromatidae) most of the flagellum has articles with subequal setal pattern; the mechanism of new article production involves the division of the first article and one further division of the articles produced by it. In I. chelipes (Idoteidae) most of the flagellum has articles with subequal setal pattern; the mechanism of new article production involves, unlike S. serratum, the division of the first article only.
The mechanism of annulation in flagellar structures and its relationship with growth at the cellular level has been studied in two models (already used for other observations previously described): the flagellum of the second antennae of A. aquaticus and the rami of the pleopods of G. roeselii. The pleopodal rami of G. roeselii increase their article number for the whole life. New articles are produced in the proximal part, by division of the first article only. In this structure, as well as in the second antennal flagellum of A. aquaticus, mitotic figures are found only in the proximal part and going distally, to "older" parts, nuclei becomes more spaced and longer. Thus, in both the models studied there is a proximal proliferative zone; cells produced there are then moved distally by the production of new cells and they go through a shape change. How this process is related to the diversity of the segmentation mechanism is not currently understood.
The production of joints and muscle insertions are developmentally correlated processes. Evidence for it was already available for the articles (except tarsomeres) of insect leg, but I have shown in this thesis this is also true for other arthropod appendages, since new joints produced during postembryonic development have also new muscle insertions, if a muscle is present. Joints without any muscle insertion can occur in arthropod appendages, but these have either no muscle passing through or just tendon(s); the occurrence of joints without any muscle insertion but with muscle(s) passing through is currently very doubtful. Thus, the traditional distinction between true article and annuli based on the presence/absence of intrinsic musculature is wrong; articles usually considered annuli may have muscle insertion. Functionally, however, this distinction is still valid, since articles with intermediate insertions of muscles parallel to the proximo-distal axis can not move the appendage independently from other articles as the other true articles (equipped with intrinsic and antagonist muscles confined within them) can do. The naupliar antennal exopod of Artemia also provide evidence that joints and muscle insertions are developmentally correlated processes. In this model there are not complete joints, but just "partial" cuticular folds, but also these (which are probably derived from a complete joint) have muscle insertions. A general difference in the timing of expression of true articles and annuli was previously noted and has been here discussed in some deep. A difference in timing exists, but it is not between true articles and annuli (if defined by the presence/absence of muscle insertions) but between articles with independent movements and articles with movements not independent to each others. Also this ontogenetic difference is connected with the different functional morphology of these articles. Flagellar structure also exhibits similarities in their postembryonic development, and these similarities are connected to the presence of a specific proximal "growth zone" (a zone where both new articles are produced and mitoses are localized). The phylogenetic distribution of this growth zone is discussed and it is here proposed to be an ancestral condition for the postembryonic development of (first) antennae and rami of postantennulary appendages of, at least, mandibulate (myriapods, insects and crustaceans) arthropods.

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EPrint type:Ph.D. thesis
Tutor:Minelli, Alessandro
Ph.D. course:Ciclo 20 > Corsi per il 20simo ciclo > BIOLOGIA EVOLUZIONISTICA
Data di deposito della tesi:2008
Anno di Pubblicazione:2008
Key Words:Arthropoda, appendages, segmentation, postembryonic development
Settori scientifico-disciplinari MIUR:Area 05 - Scienze biologiche > BIO/05 Zoologia
Struttura di riferimento:Dipartimenti > Dipartimento di Biologia
Codice ID:779
Depositato il:10 Sep 2008
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