Carlo Brena - Academia.edu (original) (raw)

Papers by Carlo Brena

PLoS biology, 2014

Myriapods (e.g., centipedes and millipedes) display a simple homonomous body plan relative to oth... more Myriapods (e.g., centipedes and millipedes) display a simple homonomous body plan relative to other arthropods. All members of the class are terrestrial, but they attained terrestriality independently of insects. Myriapoda is the only arthropod class not represented by a sequenced genome. We present an analysis of the genome of the centipede Strigamia maritima. It retains a compact genome that has undergone less gene loss and shuffling than previously sequenced arthropods, and many orthologues of genes conserved from the bilaterian ancestor that have been lost in insects. Our analysis locates many genes in conserved macro-synteny contexts, and many small-scale examples of gene clustering. We describe several examples where S. maritima shows different solutions from insects to similar problems. The insect olfactory receptor gene family is absent from S. maritima, and olfaction in air is likely effected by expansion of other receptor gene families. For some genes S. maritima has evolv...

Evolution & Development, 2005

The Hox genes are intimately involved in patterning the animal body during development and are co... more The Hox genes are intimately involved in patterning the animal body during development and are considered to have had a pivotal role in the evolution of different body plans among the metazoans. From this perspective, crustaceans, a group that has evolved an extreme diversity of body structures, represent a choice group in which to study the evolution of these genes and their expression. The expression of one of these genes, Abdominal-B (Abd-B ), has only been studied in two distantly related crustaceans, Artemia and Sacculina, where it shows dissimilar patterns, highly differentiated from the one described in other arthropods. Moreover, we have no information for the Malacostraca. Thus, we cloned the gene Abd-B and followed its expression through development by in situ hybridization in the isopod Porcellio scaber. We found a highly dynamic expression pattern of PsAbd-B during embryonic development. In early stages, it is expressed in the posterior-most part of the germ band, in a domain common to several arthropods studied to date, and later it is expressed in the developing limb buds of the pleon and still later in the endopodites of the third to fifth pleopodites. This raises the interesting possibility of the involvement of this gene in the later respiratory specialization of these appendages. In association with the above expression domain, Abd-B appears to be expressed in later stages also in the ventral ectoderm, raising the further suggestion of its possible involvement in patterning the developing nervous system. Moreover, we show that the first pleopod and the endopodite of the second pleopod, whereas present as limb buds in early embryonic stages, are later reduced and actually absent in the first postembryonic stage, although they reappear again in adults. These appendages thus represent an example of Lazarus appendages. Our data show strong plasticity in the use of a key developmental gene and point out the necessity of further research that may end with a revision of the current understanding of its role in animal evolution.

Marine Biology, 2002

The functions of the various gut regions of Oikopleura dioica (oesophagus, left and right gastric... more The functions of the various gut regions of Oikopleura dioica (oesophagus, left and right gastric lobes, vertical intestine, mid-intestine and rectum) were investigated by means of histochemical, histoenzymatic and immunohistochemical techniques at light and electron microscopes. Ciliary food progression is evidenced by the presence of ATPases on cilia, along the entire gut, with the exception of the cardiac valve, a passive device controlling food direction. Absorptive processes (alkaline phosphatase), active transport (ATPases) and nitrogen excretion (D-amino acid oxidase) occur along the entire gut, in both ciliated microvillar and globular cells. The latter, typical of the left gastric lobe and rectum, are also involved in endocytotic processes (exogenous peroxidase as tracer) and intracellular digestion (α-amylase, aminopeptidase M, acid phosphatase, 5′-nucleotidase, non-specific esterase). The giant cells of the gastric band participate in extracellular digestion; they contain secretory granules positive to various hydrolytic enzymes, the activity of which is also recognisable in faecal pellets inside the intestinal lumen. Lipid storage occurs mainly in the right gastric lobe and vertical intestine, whereas protein storage takes place in the rectal granular cells. Epithelial transport and possible osmoregulation occur along the entire gut, especially at the level of diffuse baso-lateral interdigitations, which increase the plasmalemma surface enormously, are often associated with mitochondria and possess numerous ATPase pumps. Data extend previous histological observations and hypotheses on the physiological role of the various gut regions. The remarkable and specific location of enzymatic activities and nutrient storage are in agreement with the high capacity of O. dioica to process a great quantity of food very rapidly and efficiently.

Journal of Morphology, 2003

The alimentary tract of Kowalevskia tenuis and K. oceanica, the only species of the appendiculari... more The alimentary tract of Kowalevskia tenuis and K. oceanica, the only species of the appendicularian family Kowalevskiidae, was studied both at the light and electron microscope levels and compared with species belonging to the other two families of the class. Kowalevskids show interesting specializations: 1) the pharynx opens on both sides through two opposing spiracles, modified into long ciliated fissures, and possesses an original filtering system of ciliated combs arranged in two pairs of opposing longitudinal rows; 2) the endostyle is absent, its place being taken by a ciliated groove without any glandular cell; 3) posterior to the esophagus, the globular stomach and rectum form a digestive nucleus comprising a few, large cells including two well-developed, specialized valves, cardiac and pyloric; 4) special apical junctions bearing characteristics of both gap and adherens junctions are diffuse along the gut epithelium; 5) the heart is absent. Our data suggest that Kowalevskiidae underwent a high degree of specialization for food filtering and are more closely related to Fritillariidae, with which they share several characters, rather than Oikopleuridae, the latter probably representing the most primitive family of appendicularians. J. Morphol. 258:225–238, 2003. ©2003 Wiley-Liss, Inc.

Invertebrate Biology, 2001

Abstract. The appendicularians, planktonic tunicates, possess a specialized, external filtering s... more Abstract. The appendicularians, planktonic tunicates, possess a specialized, external filtering system that captures food particles <1 μm in size. In this work the alimentary canal of Oikopleura dioica has been studied by serial sections of whole animals and ultrastructure. The gut includes a dorsal esophagus, a bilobed saccular stomach, and a curved intestine, divided into vertical, mid-, and distal intestine (or rectum). No multicellular glands or cellular proliferative centers were found. Three main cell types were recognized, ciliated microvillar cells, globular cells and gastric band cells, with specializations reflecting different physiological roles in the various regions. Ciliated microvillar cells, the most diffuse, are considered to be involved in food propulsion, fecal pellet formation, absorption, and nutrient storage. Pinocytotic features and vacuoles suggest that absorption of macromolecules and intracellular digestion occur in the globular cells of the stomach and rectum. The large gastric band cells of the left lobe have typical features of intense protein synthesis and probably produce enzymes for extracellular digestion. Diffuse interdigitations of many cells enormously increase the plasmalemma surface and may be involved in liquid/ion exchange. Despite the apparent structural simplicity of the gut epithelium, O. dioica efficiently processes food to fulfill the energy requirements of its exceptionally rapid life-cycle.

Marine Biology, 2003

The morphology and some functions of the gut of Fritillaria pellucida and Fritillaria formica (Fr... more The morphology and some functions of the gut of Fritillaria pellucida and Fritillaria formica (Fritillaridae) were investigated by light and electron microscopy, and also by means of histochemical and immunohistochemical techniques. Fritillarids, very important for their abundance and ecological impact in marine ecosystems, have a very simplified gut: a straight oesophagus connects the pharynx to the digestive nucleus, composed of globular stomach and rectum, connected dorsally through a very short proximal intestine. The latter is characterised by a few (two to four) extremely specialised cells, completely filled with mitochondria associated tightly with membrane infoldings showing strong ATP-ase activity, and probably involved in the osmoregulation of internal body fluids. The gut is formed of an extremely low number of cells, which, although poorly diversified, are very large in the stomach and rectum. Food transfer along the gut depends on and is regulated by well-developed cardiac and pyloric valves, and signs of general digestive and absorptive activity are recognisable all along the brush border of the main tracts. The macroscopic organisation and cytological characters of the gut in fritillarids are completely different from those of the oikopleurids. In particular, fritillarids lack specialised cells for endocytosis and intracellular digestion, like those described in the genus Oikopleura. The general simplification and specialisation observed in Fritillaria gut may account for their elevated growth rate and abundant diffusion in all oceans.

Zoologischer Anzeiger, 2003

In this work, we studied for the first time the histology and ultrastructure of the gut of Append... more In this work, we studied for the first time the histology and ultrastructure of the gut of Appendicularia sicula and demonstrated the absence of any trace of anus. Appendicularians are small holoplanktonic tunicates, characterised by very fast ingestion and quick food transfer along their gut. The high production of faecal pellets released in the aqueous environment, associated with a high filtration rate, highlights their important role in marine ecosystems. Due to the absence of an anus, in contrast with other appendicularians, A. sicula, one of the smallest species, accumulates undigested faecal material within its body, with consequent extreme enlargement of its rectum. The gut, the epithelium of which is generally extremely reduced, is formed of an oesophagus, a globular stomach, thin proximal and mid-intestine, and a huge rectum. The latter, when filled with faecal material, may occupy most of the volume of the trunk in fully grown specimens. Although profoundly altered, the gut of these animals does show several similarities to that of Fritillaria (a genus of the same family, Fritillariidae), with which it has in common many features such as specialised mitochondrial pump cells. In A. sicula, the structural simplifications of organs seem to reach their extreme condition in comparison to other appendicularians.

Zoologischer Anzeiger, 2003

In this work, we studied for the first time the histology and ultrastructure of the gut of Append... more In this work, we studied for the first time the histology and ultrastructure of the gut of Appendicularia sicula and demonstrated the absence of any trace of anus. Appendicularians are small holoplanktonic tunicates, characterised by very fast ingestion and quick food transfer along their gut. The high production of faecal pellets released in the aqueous environment, associated with a high filtration rate, highlights their important role in marine ecosystems. Due to the absence of an anus, in contrast with other appendicularians, A. sicula, one of the smallest species, accumulates undigested faecal material within its body, with consequent extreme enlargement of its rectum. The gut, the epithelium of which is generally extremely reduced, is formed of an oesophagus, a globular stomach, thin proximal and mid-intestine, and a huge rectum. The latter, when filled with faecal material, may occupy most of the volume of the trunk in fully grown specimens. Although profoundly altered, the gut of these animals does show several similarities to that of Fritillaria (a genus of the same family, Fritillariidae), with which it has in common many features such as specialised mitochondrial pump cells. In A. sicula, the structural simplifications of organs seem to reach their extreme condition in comparison to other appendicularians.

Development Genes and Evolution, 2006

The traditional framework for the description of arthropod development takes the molt-to-molt int... more The traditional framework for the description of arthropod development takes the molt-to-molt interval as the fundamental unit of periodization, which is similar to the morphological picture of the main body axis as a series of segments. Developmental time is described as the subdivision into a few major stages of one or more instars each, which is similar to the subdivision of the main body axis into regions of one to many segments each. Parallel to recent criticisms to the segment as the fundamental building block of arthropod anatomy, we argue that, while a firm subdivision of development in stages is useful for describing arthropod ontogeny, this is limiting as a starting point for studying its evolution. Evolutionary change affects the association between different developmental processes, some of which are continuous in time whereas others are linked to the molting cycle. Events occurring but once in life (hatching; first achieving sexual maturity) are traditionally used to establish boundaries between major units of arthropod developmental time, but these boundaries are quite labile. The presence of embryonic molts, the ‘gray zone’ of development accompanying hatching (with the frequent delivery of an immature whose qualification as ‘free-embryo’ or ordinary postembryonic stage is arbitrary), and the frequent decoupling of growth and molting suggest a different view. Beyond the simple comparison of developmental schedules in terms of heterochrony, the flexible canvas we suggest for the analysis of arthropod development opens new vistas into its evolution. Examples are provided as to the origin of holometaboly and hypermetaboly within the insects.

Evolution & Development, 2009

SUMMARY Here we address the question of how arthropod segment number may evolve by reporting the ... more SUMMARY Here we address the question of how arthropod segment number may evolve by reporting the results of further work on the model system Strigamia maritima. Recently, we showed that there was a plastic component of the variation in segment number within this species; now we demonstrate that there is also a heritable component. This is important because it enables a connection to be made between the known latitudinal trend among species of geophilomorph centipedes (more segments at lower latitudes) and the parallel trend within them. This latter trend is best documented in S. maritima but is also known in several other species. However, while a general connection between the inter- and intraspecific trends can now be made, deciding upon a specific hypothesis of the nature of the selection involved is still problematic. We provide two alternative hypotheses, one based on the temperature-related plasticity in segment number being adaptive, the other based on it being nonadaptive.

Evodevo, 2010

Background: The heads of annelids (earthworms, polychaetes, and others) and arthropods (insects, ... more Background: The heads of annelids (earthworms, polychaetes, and others) and arthropods (insects, myriapods, spiders, and others) and the arthropod-related onychophorans (velvet worms) show similar brain architecture and for this reason have long been considered homologous. However, this view is challenged by the 'new phylogeny' placing arthropods and annelids into distinct superphyla, Ecdysozoa and Lophotrochozoa, together with many other phyla lacking elaborate heads or brains. To compare the organisation of annelid and arthropod heads and brains at the molecular level, we investigated head regionalisation genes in various groups. Regionalisation genes subdivide developing animals into molecular regions and can be used to align head regions between remote animal phyla. Results: We find that in the marine annelid Platynereis dumerilii, expression of the homeobox gene six3 defines the apical region of the larval body, peripherally overlapping the equatorial otx+ expression. The six3+ and otx+ regions thus define the developing head in anterior-to-posterior sequence. In another annelid, the earthworm Pristina, as well as in the onychophoran Euperipatoides, the centipede Strigamia and the insects Tribolium and Drosophila, a six3/optix+ region likewise demarcates the tip of the developing animal, followed by a more posterior otx/otd+ region. Identification of six3+ head neuroectoderm in Drosophila reveals that this region gives rise to median neurosecretory brain parts, as is also the case in annelids. In insects, onychophorans and Platynereis, the otx + region instead harbours the eye anlagen, which thus occupy a more posterior position.

Mechanisms of Development, 2009

Evolution & Development, 2006

SUMMARY We report the coding sequence and embryonic expression of the four trunk Hox genes Antenn... more 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.

Evolution & Development, 2010

Geophilomorph centipedes show variation in segment number (a) between closely related species and... more Geophilomorph centipedes show variation in segment number (a) between closely related species and (b) within and between populations of the same species. We have previously shown for a Scottish population of the coastal centipede Strigamia maritima that the temperature of embryonic development is one of the factors that affects the segment number of hatchlings, and hence of adults, as these animals grow epimorphically—that is, without postembryonic addition of segments. Here, we show, using temperature-shift experiments, that the main developmental period during which embryos are sensitive to environmental temperature is surprisingly early, during blastoderm formation and before, or very shortly after, the onset of segmentation.

PLoS biology, 2014

Myriapods (e.g., centipedes and millipedes) display a simple homonomous body plan relative to oth... more Myriapods (e.g., centipedes and millipedes) display a simple homonomous body plan relative to other arthropods. All members of the class are terrestrial, but they attained terrestriality independently of insects. Myriapoda is the only arthropod class not represented by a sequenced genome. We present an analysis of the genome of the centipede Strigamia maritima. It retains a compact genome that has undergone less gene loss and shuffling than previously sequenced arthropods, and many orthologues of genes conserved from the bilaterian ancestor that have been lost in insects. Our analysis locates many genes in conserved macro-synteny contexts, and many small-scale examples of gene clustering. We describe several examples where S. maritima shows different solutions from insects to similar problems. The insect olfactory receptor gene family is absent from S. maritima, and olfaction in air is likely effected by expansion of other receptor gene families. For some genes S. maritima has evolv...

Evolution & Development, 2005

The Hox genes are intimately involved in patterning the animal body during development and are co... more The Hox genes are intimately involved in patterning the animal body during development and are considered to have had a pivotal role in the evolution of different body plans among the metazoans. From this perspective, crustaceans, a group that has evolved an extreme diversity of body structures, represent a choice group in which to study the evolution of these genes and their expression. The expression of one of these genes, Abdominal-B (Abd-B ), has only been studied in two distantly related crustaceans, Artemia and Sacculina, where it shows dissimilar patterns, highly differentiated from the one described in other arthropods. Moreover, we have no information for the Malacostraca. Thus, we cloned the gene Abd-B and followed its expression through development by in situ hybridization in the isopod Porcellio scaber. We found a highly dynamic expression pattern of PsAbd-B during embryonic development. In early stages, it is expressed in the posterior-most part of the germ band, in a domain common to several arthropods studied to date, and later it is expressed in the developing limb buds of the pleon and still later in the endopodites of the third to fifth pleopodites. This raises the interesting possibility of the involvement of this gene in the later respiratory specialization of these appendages. In association with the above expression domain, Abd-B appears to be expressed in later stages also in the ventral ectoderm, raising the further suggestion of its possible involvement in patterning the developing nervous system. Moreover, we show that the first pleopod and the endopodite of the second pleopod, whereas present as limb buds in early embryonic stages, are later reduced and actually absent in the first postembryonic stage, although they reappear again in adults. These appendages thus represent an example of Lazarus appendages. Our data show strong plasticity in the use of a key developmental gene and point out the necessity of further research that may end with a revision of the current understanding of its role in animal evolution.

Marine Biology, 2002

The functions of the various gut regions of Oikopleura dioica (oesophagus, left and right gastric... more The functions of the various gut regions of Oikopleura dioica (oesophagus, left and right gastric lobes, vertical intestine, mid-intestine and rectum) were investigated by means of histochemical, histoenzymatic and immunohistochemical techniques at light and electron microscopes. Ciliary food progression is evidenced by the presence of ATPases on cilia, along the entire gut, with the exception of the cardiac valve, a passive device controlling food direction. Absorptive processes (alkaline phosphatase), active transport (ATPases) and nitrogen excretion (D-amino acid oxidase) occur along the entire gut, in both ciliated microvillar and globular cells. The latter, typical of the left gastric lobe and rectum, are also involved in endocytotic processes (exogenous peroxidase as tracer) and intracellular digestion (α-amylase, aminopeptidase M, acid phosphatase, 5′-nucleotidase, non-specific esterase). The giant cells of the gastric band participate in extracellular digestion; they contain secretory granules positive to various hydrolytic enzymes, the activity of which is also recognisable in faecal pellets inside the intestinal lumen. Lipid storage occurs mainly in the right gastric lobe and vertical intestine, whereas protein storage takes place in the rectal granular cells. Epithelial transport and possible osmoregulation occur along the entire gut, especially at the level of diffuse baso-lateral interdigitations, which increase the plasmalemma surface enormously, are often associated with mitochondria and possess numerous ATPase pumps. Data extend previous histological observations and hypotheses on the physiological role of the various gut regions. The remarkable and specific location of enzymatic activities and nutrient storage are in agreement with the high capacity of O. dioica to process a great quantity of food very rapidly and efficiently.

Journal of Morphology, 2003

The alimentary tract of Kowalevskia tenuis and K. oceanica, the only species of the appendiculari... more The alimentary tract of Kowalevskia tenuis and K. oceanica, the only species of the appendicularian family Kowalevskiidae, was studied both at the light and electron microscope levels and compared with species belonging to the other two families of the class. Kowalevskids show interesting specializations: 1) the pharynx opens on both sides through two opposing spiracles, modified into long ciliated fissures, and possesses an original filtering system of ciliated combs arranged in two pairs of opposing longitudinal rows; 2) the endostyle is absent, its place being taken by a ciliated groove without any glandular cell; 3) posterior to the esophagus, the globular stomach and rectum form a digestive nucleus comprising a few, large cells including two well-developed, specialized valves, cardiac and pyloric; 4) special apical junctions bearing characteristics of both gap and adherens junctions are diffuse along the gut epithelium; 5) the heart is absent. Our data suggest that Kowalevskiidae underwent a high degree of specialization for food filtering and are more closely related to Fritillariidae, with which they share several characters, rather than Oikopleuridae, the latter probably representing the most primitive family of appendicularians. J. Morphol. 258:225–238, 2003. ©2003 Wiley-Liss, Inc.

Invertebrate Biology, 2001

Abstract. The appendicularians, planktonic tunicates, possess a specialized, external filtering s... more Abstract. The appendicularians, planktonic tunicates, possess a specialized, external filtering system that captures food particles <1 μm in size. In this work the alimentary canal of Oikopleura dioica has been studied by serial sections of whole animals and ultrastructure. The gut includes a dorsal esophagus, a bilobed saccular stomach, and a curved intestine, divided into vertical, mid-, and distal intestine (or rectum). No multicellular glands or cellular proliferative centers were found. Three main cell types were recognized, ciliated microvillar cells, globular cells and gastric band cells, with specializations reflecting different physiological roles in the various regions. Ciliated microvillar cells, the most diffuse, are considered to be involved in food propulsion, fecal pellet formation, absorption, and nutrient storage. Pinocytotic features and vacuoles suggest that absorption of macromolecules and intracellular digestion occur in the globular cells of the stomach and rectum. The large gastric band cells of the left lobe have typical features of intense protein synthesis and probably produce enzymes for extracellular digestion. Diffuse interdigitations of many cells enormously increase the plasmalemma surface and may be involved in liquid/ion exchange. Despite the apparent structural simplicity of the gut epithelium, O. dioica efficiently processes food to fulfill the energy requirements of its exceptionally rapid life-cycle.

Marine Biology, 2003

The morphology and some functions of the gut of Fritillaria pellucida and Fritillaria formica (Fr... more The morphology and some functions of the gut of Fritillaria pellucida and Fritillaria formica (Fritillaridae) were investigated by light and electron microscopy, and also by means of histochemical and immunohistochemical techniques. Fritillarids, very important for their abundance and ecological impact in marine ecosystems, have a very simplified gut: a straight oesophagus connects the pharynx to the digestive nucleus, composed of globular stomach and rectum, connected dorsally through a very short proximal intestine. The latter is characterised by a few (two to four) extremely specialised cells, completely filled with mitochondria associated tightly with membrane infoldings showing strong ATP-ase activity, and probably involved in the osmoregulation of internal body fluids. The gut is formed of an extremely low number of cells, which, although poorly diversified, are very large in the stomach and rectum. Food transfer along the gut depends on and is regulated by well-developed cardiac and pyloric valves, and signs of general digestive and absorptive activity are recognisable all along the brush border of the main tracts. The macroscopic organisation and cytological characters of the gut in fritillarids are completely different from those of the oikopleurids. In particular, fritillarids lack specialised cells for endocytosis and intracellular digestion, like those described in the genus Oikopleura. The general simplification and specialisation observed in Fritillaria gut may account for their elevated growth rate and abundant diffusion in all oceans.

Zoologischer Anzeiger, 2003

In this work, we studied for the first time the histology and ultrastructure of the gut of Append... more In this work, we studied for the first time the histology and ultrastructure of the gut of Appendicularia sicula and demonstrated the absence of any trace of anus. Appendicularians are small holoplanktonic tunicates, characterised by very fast ingestion and quick food transfer along their gut. The high production of faecal pellets released in the aqueous environment, associated with a high filtration rate, highlights their important role in marine ecosystems. Due to the absence of an anus, in contrast with other appendicularians, A. sicula, one of the smallest species, accumulates undigested faecal material within its body, with consequent extreme enlargement of its rectum. The gut, the epithelium of which is generally extremely reduced, is formed of an oesophagus, a globular stomach, thin proximal and mid-intestine, and a huge rectum. The latter, when filled with faecal material, may occupy most of the volume of the trunk in fully grown specimens. Although profoundly altered, the gut of these animals does show several similarities to that of Fritillaria (a genus of the same family, Fritillariidae), with which it has in common many features such as specialised mitochondrial pump cells. In A. sicula, the structural simplifications of organs seem to reach their extreme condition in comparison to other appendicularians.

Zoologischer Anzeiger, 2003

In this work, we studied for the first time the histology and ultrastructure of the gut of Append... more In this work, we studied for the first time the histology and ultrastructure of the gut of Appendicularia sicula and demonstrated the absence of any trace of anus. Appendicularians are small holoplanktonic tunicates, characterised by very fast ingestion and quick food transfer along their gut. The high production of faecal pellets released in the aqueous environment, associated with a high filtration rate, highlights their important role in marine ecosystems. Due to the absence of an anus, in contrast with other appendicularians, A. sicula, one of the smallest species, accumulates undigested faecal material within its body, with consequent extreme enlargement of its rectum. The gut, the epithelium of which is generally extremely reduced, is formed of an oesophagus, a globular stomach, thin proximal and mid-intestine, and a huge rectum. The latter, when filled with faecal material, may occupy most of the volume of the trunk in fully grown specimens. Although profoundly altered, the gut of these animals does show several similarities to that of Fritillaria (a genus of the same family, Fritillariidae), with which it has in common many features such as specialised mitochondrial pump cells. In A. sicula, the structural simplifications of organs seem to reach their extreme condition in comparison to other appendicularians.

Development Genes and Evolution, 2006

The traditional framework for the description of arthropod development takes the molt-to-molt int... more The traditional framework for the description of arthropod development takes the molt-to-molt interval as the fundamental unit of periodization, which is similar to the morphological picture of the main body axis as a series of segments. Developmental time is described as the subdivision into a few major stages of one or more instars each, which is similar to the subdivision of the main body axis into regions of one to many segments each. Parallel to recent criticisms to the segment as the fundamental building block of arthropod anatomy, we argue that, while a firm subdivision of development in stages is useful for describing arthropod ontogeny, this is limiting as a starting point for studying its evolution. Evolutionary change affects the association between different developmental processes, some of which are continuous in time whereas others are linked to the molting cycle. Events occurring but once in life (hatching; first achieving sexual maturity) are traditionally used to establish boundaries between major units of arthropod developmental time, but these boundaries are quite labile. The presence of embryonic molts, the ‘gray zone’ of development accompanying hatching (with the frequent delivery of an immature whose qualification as ‘free-embryo’ or ordinary postembryonic stage is arbitrary), and the frequent decoupling of growth and molting suggest a different view. Beyond the simple comparison of developmental schedules in terms of heterochrony, the flexible canvas we suggest for the analysis of arthropod development opens new vistas into its evolution. Examples are provided as to the origin of holometaboly and hypermetaboly within the insects.

Evolution & Development, 2009

SUMMARY Here we address the question of how arthropod segment number may evolve by reporting the ... more SUMMARY Here we address the question of how arthropod segment number may evolve by reporting the results of further work on the model system Strigamia maritima. Recently, we showed that there was a plastic component of the variation in segment number within this species; now we demonstrate that there is also a heritable component. This is important because it enables a connection to be made between the known latitudinal trend among species of geophilomorph centipedes (more segments at lower latitudes) and the parallel trend within them. This latter trend is best documented in S. maritima but is also known in several other species. However, while a general connection between the inter- and intraspecific trends can now be made, deciding upon a specific hypothesis of the nature of the selection involved is still problematic. We provide two alternative hypotheses, one based on the temperature-related plasticity in segment number being adaptive, the other based on it being nonadaptive.

Evodevo, 2010

Background: The heads of annelids (earthworms, polychaetes, and others) and arthropods (insects, ... more Background: The heads of annelids (earthworms, polychaetes, and others) and arthropods (insects, myriapods, spiders, and others) and the arthropod-related onychophorans (velvet worms) show similar brain architecture and for this reason have long been considered homologous. However, this view is challenged by the 'new phylogeny' placing arthropods and annelids into distinct superphyla, Ecdysozoa and Lophotrochozoa, together with many other phyla lacking elaborate heads or brains. To compare the organisation of annelid and arthropod heads and brains at the molecular level, we investigated head regionalisation genes in various groups. Regionalisation genes subdivide developing animals into molecular regions and can be used to align head regions between remote animal phyla. Results: We find that in the marine annelid Platynereis dumerilii, expression of the homeobox gene six3 defines the apical region of the larval body, peripherally overlapping the equatorial otx+ expression. The six3+ and otx+ regions thus define the developing head in anterior-to-posterior sequence. In another annelid, the earthworm Pristina, as well as in the onychophoran Euperipatoides, the centipede Strigamia and the insects Tribolium and Drosophila, a six3/optix+ region likewise demarcates the tip of the developing animal, followed by a more posterior otx/otd+ region. Identification of six3+ head neuroectoderm in Drosophila reveals that this region gives rise to median neurosecretory brain parts, as is also the case in annelids. In insects, onychophorans and Platynereis, the otx + region instead harbours the eye anlagen, which thus occupy a more posterior position.

Mechanisms of Development, 2009

Evolution & Development, 2006

SUMMARY We report the coding sequence and embryonic expression of the four trunk Hox genes Antenn... more 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.

Evolution & Development, 2010

Geophilomorph centipedes show variation in segment number (a) between closely related species and... more Geophilomorph centipedes show variation in segment number (a) between closely related species and (b) within and between populations of the same species. We have previously shown for a Scottish population of the coastal centipede Strigamia maritima that the temperature of embryonic development is one of the factors that affects the segment number of hatchlings, and hence of adults, as these animals grow epimorphically—that is, without postembryonic addition of segments. Here, we show, using temperature-shift experiments, that the main developmental period during which embryos are sensitive to environmental temperature is surprisingly early, during blastoderm formation and before, or very shortly after, the onset of segmentation.