Invertebrate Lineages Research Articles

Ecomorphological analysis of aerial performance in a non-specialized lacertid lizard,Holaspis guentheri

Controlled aerial descent has evolved at least 30 times independently in different vertebrate and invertebrate lineages. A whole suite of morphological modifications, such as patagia, lateral skin folds and webbed feet, have been suggested to enhance descending ability. In this study, we compare aerial performance (i.e. vertical and horizontal velocity, horizontal distance covered, duration of descent) and morphology (body mass, body width, inter limb distance, surface area and wing loading) among three species of lizards, representing a range of aerial descenders present within the clade. Our performance measurements show that the lacertid Holaspis guentheri performs intermediately to the specialized gekkonid Ptychozoon kuhli and the rock-dwelling lizard Podarcis muralis. The small relative body mass of H. guentheri results in a low wing loading similar to that of P. kuhli thus enhancing its aerial performance. Whereas the latter generates great lift forces and is able to cover great horizontal distances, H. guentheri's low wing loading seems to be responsible for a slow descent and low impact forces upon landing. Our results show that very small morphological changes may result in noticeable and ecologically relevant changes in performance.

Gonadotropin-Releasing Hormone Receptors: Where Did They Come From?

Pope got it right, although amphioxus is a slimy ancestor to acknowledge. But what does this beast have to tell us about our origins? In this issue, Tello and Sherwood (1) propose that in amphioxus, the most basal chordate, four GnRH receptors are present: two that sit at the base of the invertebrate lineage and two at the base of the vertebrate lineage. Amphioxus, also known as the lancelet, grows to about 5 cm, has a dorsal nerve cord and other vertebrate characteristics including segmentedmuscles, a tail, andpharyngeal slits.Amphioxi live in the sand in tropical regions and, despite their evolutionary importance, are now primarily a food source. The simultaneous presence of two GnRH receptor lineages in this organism is remarkable, because it hints that amphioxus might contain similar kinds of evidence about other aspects of early vertebrate evolution. For a ligand to act, it must have a cognate receptor, and one of the most important ligands in vertebrates is GnRH1. The hypothalamus secretes GnRH1, the peptide that controls reproduction in all vertebrates. GnRH was predicted to exist in 1950 (2), but because there are only minute amounts, and the peptide has modified N and C termini, it was difficult to isolate. Twenty years later, it was structurally identified, and 12 yr after that, in 1984, the gene encoding GnRH was first described for humans (3) and rats (4). Seven years later, the first cDNA encoding GnRH in a nonmammalian species was identified in a teleost fish, leading to subsequent discoveries in that same species of three distinct genes encoding three different GnRH decapeptides and localized in spatially distinct brain areas (5). The discovery of a second form of GnRH in humans and the associated phylogenetic analysis showed that the three GnRH gene families then known formed a tidy tree, suggesting a common origin via gene duplication and that then a subsequent loss of one form was the likely evolutionary path to extant GnRH forms (6). Since then, the lamprey GnRH form has been fitted into a fourth category of GnRH molecules and the protostomian GnRHs placed into yet another lineage (7). In most species, GnRH forms are localized to particular brain areas. But GnRH peptides cannot function without cognate receptors. And the two to three GnRH forms are not matched to specific receptor types in any vertebrate where they have been identified, but rather each GnRH can bind to either of the two receptors expressed in most vertebrates. Consequently, the GnRH receptor identities and functions have been somewhat complex to understand and place into reliable families (cf. Ref. 8). These receptors seem to have been duplicated and in some cases acquired new functions during evolution. But the Tello and Sherwood (1) report suggests that at the dawn of vertebrates, things might have been more distinct. Amphioxus (Branchiostoma floridae) is the most basal chordate, but it is also classified as an invertebrate. This schizophrenic origin is supported by results showing that amphioxus has four GnRH receptors: two paralogous pairs with one phylogenetically grouped with the vertebrate GnRH receptors and the other grouped with the invertebrate (octopus) GnRH-like receptors (Fig. 4 in Ref. 1). Even more interesting, the vertebrate GnRH forms, GnRH1 and GnRH2, activate the vertebrate-type GnRH receptors, and correspondingly, an octopus GnRH-like peptide and related receptor for insect adipokinetic hormone (AKH) induced inositol phosphate pathway turnover in one of the two amphioxus receptors. So it appears that there is functional conservation from amphioxus through the vertebrate lineage. The authors infer that the mollusk GnRH-like receptor was lost somewhere in the vertebrate lineage and that one of the vertebrate-like receptors gave rise to all subsequent vertebrate GnRH receptors. Independently, Chambery et al. (9) identified a putative GnRH in amphioxus using reverse-phase chromatography. The

The Green-absorbing Drosophila Rh6 Visual Pigment Contains a Blue-shifting Amino Acid Substitution That Is Conserved in Vertebrates

The molecular mechanisms that regulate invertebrate visual pigment absorption are poorly understood. Through sequence analysis and functional investigation of vertebrate visual pigments, numerous amino acid substitutions important for this adaptive process have been identified. Here we describe a serine/alanine (S/A) substitution in long wavelength-absorbing Drosophila visual pigments that occurs at a site corresponding to Ala-292 in bovine rhodopsin. This S/A substitution accounts for a 10-17-nm absorption shift in visual pigments of this class. Additionally, we demonstrate that substitution of a cysteine at the same site, as occurs in the blue-absorbing Rh5 pigment, accounts for a 4-nm shift. Substitutions at this site are the first spectrally significant amino acid changes to be identified for invertebrate pigments sensitive to visible light and are the first evidence of a conserved tuning mechanism in vertebrate and invertebrate pigments of this class.

Independent Mammalian Genome Contractions Following the KT Boundary

Although it is generally accepted that major changes in the earth's history are significant drivers of phylogenetic diversification and extinction, such episodes may also have long-lasting effects on genomic architecture. Here we show that widespread reductions in genome size have occurred in multiple lineages of mammals subsequent to the Cretaceous–Tertiary (KT) boundary, whereas there is no evidence for such changes in other vertebrate, invertebrate, or land plant lineages. Although the mechanisms remain unclear, such shifts in mammalian genome evolution may be a consequence of an increase in the efficiency of selection against excess DNA resulting from post-KT population size expansions. Independent historical changes in genome architecture in diverse lineages raise a significant challenge to the idea that genome size is finely tuned to achieve adaptive phenotypic modifications and suggest that attempts to use phylogenetic analysis to infer ancestral genome sizes may be problematical.

The molecular ancestry of segmentation mechanisms

In 1830 a very important debate on natural history took place in the French Academy of Sciences. As retold in enjoyable detail by T. A. Appel (1), the adversaries were Georges Cuvier and Etienne Geoffroy Saint-Hilaire. These were pre-Darwinian times—the Origin of Species was published in 1859—so their arguments sound antiquated today, but their reverberations among biological ideas have continued to the present day. Cuvier, the discoverer of extinction, held the view that animal anatomy was determined by the functional purpose of each organ, which he called the “conditions of existence.” Geoffroy, the discoverer of “analogies” (now called homologies), held that animal anatomy had a “unity of plan” upon which thousands of variations were imposed. He compared vertebrates to arthropods, arguing that they shared antero–posterior (A–P) characteristics, such as head, thorax, and abdomen, as well as dorsal–ventral (D–V) landmarks such as a CNS, gastrointestinal tract, and heart, except that a D-V inversion of the body plan had occurred. Geoffroy even had the temerity of comparing the segmentation of arthropods to that of vertebrates. Cuvier presented the better arguments and was considered the victor of the debate. However, modern evolution and development studies have discovered that common genetic networks pattern the A–P and D–V axes of very distantly related bilateral animals (2, 3). This realization has provided a measure of molecular support for Geoffroy's unity of plan hypothesis and for the idea that the last common ancestor of the invertebrate and vertebrate lineages was a rather complex animal, called Urbilateria (which means primeval bilateral animal), which predated the Cambrian explosion that took place 535–525 million years ago (3). In this issue of PNAS, Pueyo et al. (4) make an important contribution to the question of whether common mechanisms of segmentation are shared by insects and vertebrates (5, 6).

The antiquity of Madagascar’s grasslands and the rise of C4 grassy biomes

AbstractAim Grasslands and savannas, which make up > 75% of Madagascar’s land area, have long been viewed as anthropogenically derived after people settled on the island c. 2 ka. We investigated this hypothesis and an alternative – that the grasslands are an insular example of the post‐Miocene spread of C4 grassy biomes world‐wide.Location Madagascar, southern Africa, East Africa.Methods We compared the number of C4 grass genera in Madagascar with that in southern and south‐central African floras. If the grasslands are recent we would expect to find fewer species and genera in Madagascar relative to Africa and for these species and genera to have very wide distribution ranges in Madagascar. Secondly, we searched Madagascan floras for the presence of endemic plant species or genera restricted to grasslands. We also searched for evidence of a grassland specialist fauna with species endemic to Madagascar. Plant and animal species endemic to C4 grassy biomes would not be expected if these are of recent origin.Results Madagascar has c. 88 C4 grass genera, including six endemic genera. Excluding African genera with only one or two species, Madagascar has 86.6% of southern Africa’s and 89.4% of south‐central Africa’s grass genera. C4 grass species make up c. 4% of the flora of both Madagascar and southern Africa and species : genus ratios are similar (4.3 and 5.1, respectively). Turnover of grasses along geographical gradients follows similar patterns to those in South Africa, with Andropogoneae dominating in mesic biomes and Chlorideae in semi‐arid grassy biomes. At least 16 monocot genera have grassland members, many of which are endemic to Madagascar. Woody species in frequently burnt savannas include both Madagascan endemics and African species. A different woody flora, mostly endemic, occurs in less frequently burnt grasslands in the central highlands, filling a similar successional niche to montane C4 grasslands in Africa. Diverse vertebrate and invertebrate lineages have grassland specialists, including many endemic to Madagascar (e.g. termites, ants, lizards, snakes, birds and mammals). Grassland use of the extinct fauna is poorly known but carbon isotope analysis indicates that a hippo, two giant tortoises and one extinct lemur ate C4 or CAM (crassulacean acid metabolism) plants.Main conclusions The diversity of C4 grass lineages in Madagascar relative to that in Africa, and the presence of plant and animal species endemic to Madagascan grassy biomes, does not fit the view that these grasslands are anthropogenically derived. We suggest that grasslands invaded Madagascar after the late Miocene, part of the world‐wide expansion of C4 grassy biomes. Madagascar provides an interesting test case for biogeographical analysis of how these novel biomes assembled, and the sources of the flora and fauna that now occupy them. A necessary part of such an analysis would be to establish the pre‐settlement extent of the C4 grassy biomes. Carbon isotope analysis of soil organic matter would be a feasible method for doing this.

Ecosystem-wide body-size trends in Cambrian–Devonian marine invertebrate lineages

Fossil marine lineages are generally expected to exhibit long-term trends of increasing body size because of inherent fitness advantages or secular changes in environmental conditions. Because empirical documentation of this trend during the Paleozoic has been lacking for most taxonomic groups, the magnitude, timing, and taxonomic breadth of the trend have remained elusive. This study uses the largest existing database of fossil invertebrate sizes from four faunally important phyla to document ecosystem-wide size trends in well-preserved biotas from deep-subtidal, soft-substrate assemblages during the Cambrian through Devonian. Size of type specimens was measured along standard body axes from monographic plates and converted to body volume by using a broadly applicable empirical regression. Results demonstrate that mean body size (herein volume) of individual genera doubles during this interval, especially from the Late Ordovician through Early Devonian. The timing is gradual in spite of major radiations and extinctions, and the increase is primarily attributable to a net increase in the three-dimensionality of genera. The overall increase is not caused by replacement among clades because increases are widespread among arthropods, brachiopods, and echinoderms, at the phylum and class levels; in contrast, mollusks do not display a net size change at either taxonomic level. The increase is also more pronounced in microbivores than in carnivores. Combined with known environmental changes during this interval, and especially records of carbon dioxide, these trends provide support for the claim that primary productivity increased during the early to mid Paleozoic.

Selection for Social Signalling Drives the Evolution of Chameleon Colour Change

Rapid colour change is a remarkable natural phenomenon that has evolved in several vertebrate and invertebrate lineages. The two principal explanations for the evolution of this adaptive strategy are (1) natural selection for crypsis (camouflage) against a range of different backgrounds and (2) selection for conspicuous social signals that maximise detectability to conspecifics, yet minimise exposure to predators because they are only briefly displayed. Here we show that evolutionary shifts in capacity for colour change in southern African dwarf chameleons (Bradypodion spp.) are associated with increasingly conspicuous signals used in male contests and courtship. To the chameleon visual system, species showing the most dramatic colour change display social signals that contrast most against the environmental background and amongst adjacent body regions. We found no evidence for the crypsis hypothesis, a finding reinforced by visual models of how both chameleons and their avian predators perceive chameleon colour variation. Instead, our results suggest that selection for conspicuous social signals drives the evolution of colour change in this system, supporting the view that transitory display traits should be under strong selection for signal detectability.

Are we degenerate tetraploids? More genomes, new facts

BackgroundWithin the bilaterians, the appearance and evolution of vertebrates is accompanied by enormous changes in anatomical, morphological and developmental features. This evolution of increased complexity has been associated with two genome duplications (2R hypothesis) at the origin of vertebrates. However, in spite of extensive debate the validity of the 2R hypothesis remains controversial. The paucity of sequence data in early years of genomic era was an intrinsic obstacle in tracking the genome evolutionary history of chordates.HypothesisIn this article I review the 2R hypothesis by taking into account the recent availability of genomic sequence data for an expanding range of animals. I argue here that genetic architecture of lower metazoans and representatives of major vertebrate and invertebrate lineages provides no support for the hypothesis relating the origin of vertebrates with widespread gene or genome duplications.ConclusionIt appears that much of the genomic complexity of modern vertebrates is very ancient likely predating the origin of chordates or even the Bilaterian-Nonbilaterian divergence. The origin and evolution of vertebrates is partly accompanied by an increase in gene number. However, neither can we take this subtle increase in gene number as an only causative factor for evolution of phenotypic complexity in modern vertebrates nor we can take it as a reflection of polyplodization events early in their history.ReviewersThis article was reviewed by Eugene Koonin, Joshua Cherry (nominated by David Lipman), and Jerzy Jurka.

A Common Ankyrin-G-Based Mechanism Retains KCNQ and NaVChannels at Electrically Active Domains of the Axon

KCNQ (KV7) potassium channels underlie subthreshold M-currents that stabilize the neuronal resting potential and prevent repetitive firing of action potentials. Here, antibodies against four different KCNQ2 and KCNQ3 polypeptide epitopes show these subunits concentrated at the axonal initial segment (AIS) and node of Ranvier. AIS concentration of KCNQ2 and KCNQ3, like that of voltage-gated sodium (NaV) channels, is abolished in ankyrin-G knock-out mice. A short motif, common to KCNQ2 and KCNQ3, mediates both in vivo ankyrin-G interaction and retention of the subunits at the AIS. This KCNQ2/KCNQ3 motif is nearly identical to the sequence on NaV alpha subunits that serves these functions. All identified NaV and KCNQ genes of worms, insects, and molluscs lack the ankyrin-G binding motif. In contrast, vertebrate orthologs of NaV alpha subunits, KCNQ2, and KCNQ3 (including from bony fish, birds, and mammals) all possess the motif. Thus, concerted ankyrin-G interaction with KCNQ and NaV channels appears to have arisen through convergent molecular evolution, after the division between invertebrate and vertebrate lineages, but before the appearance of the last common jawed vertebrate ancestor. This includes the historical period when myelin also evolved.

FOXO-independent suppression of programmed cell death by the PI3K/Akt signaling pathway in Drosophila

Signaling through the PI3K/Akt/FOXO pathway plays an important role in vertebrates in protecting cells from programmed cell death. PI3K and Akt have been similarly shown to be involved in survival signaling in the invertebrate model organism Drosophila. However, it is not known whether PI3K and Akt execute this function by controlling a pro-apoptotic activity of Drosophila FOXO. In this study, we show that elevated signaling through PI3K and Akt can prevent developmentally controlled death in the salivary glands of the fruit fly. We further show that Drosophila FOXO is not required for normal salivary gland death and that the rescue of salivary gland death by PI3K occurs independent of FOXO. These results give support to the notion that FOXOs have acquired pro-apoptotic functions after separation of the vertebrate and invertebrate lineages.

Biodiversity in Sri Lanka and the Western Ghats

We read with interest the Report “Local endemism within the Western Ghats-Sri Lanka biodiversity hotspot” by F. Bossuyt et al. (15 Oct. 2004, p. [479][1]), which documents patterns of diversification in selected vertebrate and invertebrate lineages from Sri Lanka and the Western Ghats region of

Characterization of multiple lineages of Tc1-like elements within the genome of the amphibian Xenopus tropicalis

We have used genomic sequencing data extracted from the first assembly of the Xenopus tropicalis genome combined with a degenerated PCR approach to identify multiple lineages of Tc1 related transposable elements. Full-length elements were isolated in each lineage and were characterized. Most of them exhibit the typical characteristics of Tc1-like elements ( TLEs). An open reading frame (ORF) encoding a 340–350 aa transposase containing a [D, D(34)E] signature was found as well as conserved inverted terminal repeats (ITRs) at each extremities. These ITRs could vary in length, depending on the TLE lineage. These new TLEs were named Eagle, Froggy, Jumpy, Maya, Xeminos, XtTXr and XtTXz. Phylogenetic analyses indicate that their closest relatives are present in the genomes of actinopterygian and amphibian. Interestingly, Maya and Xeminos share remarkable characteristics. Maya contains a [D,D(36)E] motif but is not related to any described TLE so far. Xeminos is the first vertebrate TLE strongly related to an invertebrate lineage. Finally, we have identified for most of these TLEs, copies containing an intact transposase ORF suggesting that these elements may still be active.

The nature and significance of invertebrate cartilages revisited: distribution and histology of cartilage and cartilage-like tissues within the Metazoa

Tissues similar to vertebrate cartilage have been described throughout the Metazoa. Often the designation of tissues as cartilage within non-vertebrate lineages is based upon sparse supporting data. To be considered cartilage, a tissue should meet a number of histological criteria that include composition and organization of the extracellular matrix. To re-evaluate the distribution and structural properties of these tissues, we have re-investigated the histological properties of many of these tissues from fresh material, and review the existing literature on invertebrate cartilages. Chondroid connective tissue is common amongst invertebrates, and differs from invertebrate cartilage in the structure and organization of the cells that comprise it. Groups having extensive chondroid connective tissue include brachiopods, polychaetes, and urochordates. Cartilage is found within cephalopod mollusks, chelicerate arthropods and sabellid polychaetes. Skeletal tissues found within enteropneust hemichordates are unique in that the extracellular matrix shares many properties with vertebrate cartilage, yet these tissues are completely acellular. The possibility that this tissue may represent a new category of cartilage, acellular cartilage, is discussed. Immunoreactivity of some invertebrate cartilages with antibodies that recognize molecules specific to vertebrate bone suggests an intermediate phenotype between vertebrate cartilage and bone. Although cartilage is found within a number of invertebrate lineages, we find that not all tissues previously reported to be cartilage have the appropriate properties to merit their distinction as cartilage.

EST Analysis of the Cnidarian Acropora millepora Reveals Extensive Gene Loss and Rapid Sequence Divergence in the Model Invertebrates

A significant proportion of mammalian genes are not represented in the genomes of Drosophila, Caenorhabditis or Saccharomyces, and many of these are assumed to have been vertebrate innovations. To test this assumption, we conducted a preliminary EST project on the anthozoan cnidarian, Acropora millepora, a basal metazoan. More than 10% of the Acropora ESTs with strong metazoan matches to the databases had clear human homologs but were not represented in the Drosophila or Caenorhabditis genomes; this category includes a surprising diversity of transcription factors and metabolic proteins that were previously assumed to be restricted to vertebrates. Consistent with higher rates of divergence in the model invertebrates, three-way comparisons show that most Acropora ESTs match human sequences much more strongly than they do any Drosophila or Caenorhabditis sequence. Gene loss has thus been much more extensive in the model invertebrate lineages than previously assumed and, as a consequence, some genes formerly thought to be vertebrate inventions must have been present in the common metazoan ancestor. The complexity of the Acropora genome is paradoxical, given that this organism contains apparently few tissue types and the simplest extant nervous system consisting of a morphologically homogeneous nerve net.

Molecular Basis for Ultraviolet Vision in Invertebrates

Invertebrates are sensitive to a broad spectrum of light that ranges from UV to red. Color sensitivity in the UV plays an important role in foraging, navigation, and mate selection in both flying and terrestrial invertebrate animals. Here, we show that a single amino acid polymorphism is responsible for invertebrate UV vision. This residue (UV: lysine vs blue:asparagine or glutamate) corresponds to amino acid position glycine 90 (G90) in bovine rhodopsin, a site affected in autosomal dominant human congenital night blindness. Introduction of the positively charged lysine in invertebrates is likely to deprotonate the Schiff base chromophore and produce an UV visual pigment. This same position is responsible for regulating UV versus blue sensitivity in several bird species, suggesting that UV vision has arisen independently in invertebrate and vertebrate lineages by a similar molecular mechanism.

The first non-LTR retrotransposon characterised in the cephalochordate amphioxus, BfCR1, shows similarities to CR1-like elements.

BfCR1 is the first non-long terminal repeat retrotransposon to be characterised in the amphioxus genome. Sequence alignment of the predicted translation product reveals that BfCR1 belongs to the CR1-like retroposon class, a family widely distributed in vertebrate and invertebrate lineages. Structural analysis shows conservation of the specific motifs of the ORF2-CR1 elements: the N-terminal endonuclease, the reverse transcriptase and the C-terminal domains. The BfCR1 element possesses an atypical 3' terminus consisting of the tandem repeat (AAG)6. We gathered evidence supporting the mobility of this element and report an estimated 15 copies of BfCR1, mostly truncated, per haploid genome, a remarkably low number when compared to that of vertebrates. Phylogenetic analysis, including the amphioxus element, seems to indicate that (i) CR1-like retroposons cluster in a monophyletic group and (ii) the CR1-like family was already present in the chordate ancestor. Our data provide further support for the horizontal transmission of CR1-like elements during early vertebrate evolution.

Cellular diversity in the developing nervous system: a temporal view from Drosophila.

This article considers the evidence for temporal transitions in CNS neural precursor cell gene expression during development. In Drosophila, five prospective competence states have so far been identified, characterized by the successive expression of Hb-->Kr-->Pdm-->Cas-->Gh in many, but not all, neuroblasts. In each temporal window of transcription factor expression, the neuroblast generates sublineages whose temporal identity is determined by the competence state of the neuroblast at the time of birth of the sublineage. Although similar regulatory programs have not yet been identified in mammals, candidate regulatory genes have been identified. Further investigation of the genetic programs that guide both invertebrate and vertebrate neural precursor cell lineage development will ultimately lead to an understanding of the molecular events that control neuronal diversity.

Proneural genes and the specification of neural cell types.

Certain morphological, physiological and molecular characteristics are shared by all neurons. However, despite these similarities, neurons constitute the most diverse cell population of any organism. Recently, considerable attention has been focused on identifying the molecular mechanisms that underlie this cellular diversity. Parallel studies in Drosophila and vertebrates have revealed that proneural genes are key regulators of neurogenesis, coordinating the acquisition of a generic neuronal fate and of specific subtype identities that are appropriate for the location and time of neuronal generation. These studies reveal that, in spite of differences between invertebrate and vertebrate neural lineages, Drosophila and vertebrate proneural genes have remarkably similar roles.

Gaseous Transmission Across Time and Species1

This paper reviews comparative and evolutionary aspects of nitric oxide (NO) signaling in major systematic groups such as prokaryotes, plants, fungi and invertebrate animals. It appears that NO-mediated signaling can be as old as cellular organization itself. Both non-enzymatic and enzymatic (in addition to NOS) synthetic pathways can contribute to NO formation in living systems. The evolutionary roots of this means of gaseous signaling can be traced back to the role of NO in non-immune defensive mechanisms and the role of NO in control of gene expression, chemical ecology and, perhaps, symbiotic interactions in the ancient prokaryotic world. These functions of NO can be preserved in practically all modern taxons and be widely expressed in the nervous system. However, it is hypothesized that neuronal NO signaling is a relatively new evolutionary invention and it is likely to have happened several times during animal evolution. Although a comparative analysis of neuronal NO signaling is still in its early stages, the hypothesis is proposed that in many invertebrate lineages one of the primary neuronal functions of NO was regulation of feeding patterns, chemosensory processing and neurodevelopment.