Developmental Characters Research Articles

Molecular genetic identification of crustose representatives of the order Corallinales (Rhodophyta) in Chile

Knowledge on species of the order Corallinales along the coast of Chile is still scarce despite a number of studies and records of other divisions of seaweeds made since the early 20th century. This lack of information is more dramatic among crustose representatives of the order, thus depriving biogeographic studies of a thorough analysis and resulting in inadequately representative accounts of biodiversity. The currently changing taxonomy of the group makes it difficult to identify and differentiate among taxa based on morphological and developmental characters. Therefore, the use of molecular tools has been adopted in this study in order to facilitate identification and comparison of crustose corallines collected at the rocky intertidal between 27° and 48°S along the Pacific temperate coast of South America. A sequence 600 bp (in length) from the SSU-rDNA gene was used to identify five taxa to the genus level: Lithophyllum, Spongites, Mesophyllum, Synarthrophyton, and Leptophytum. In all cases, the genus distinction based on morphological characters coincide with designations based on variation in the ribosomal DNA gene sequence. Spongites is the most frequently occurring genus and is found in all localities sampled while the others appear occasionally. Taxa recognition at species level must be examined with caution considering that morphological variability is not well understood in Chile because the SSU-rDNA region sequence does not always stand alone as an unambiguous means of identifying all coralline species. In such cases, more rapidly evolving markers are needed. For example, sequences from the ITS (rDNA) region often provide greater resolution among closely related species and genera. However, the methodology presented here remains a useful tool for species-level identification.

Developmental and genetic evidence for the existence of three morphologically cryptic species of Crepidula in northern Chile

The taxonomy of Crepidula has been based principally on shell morphology, but shell characteristics in this genus may be strongly influenced by the substrates they inhabit and are thus of limited use in classification. Four species in this genus are currently recognized from the Chilean coast, of which two, Crepidula dilatata and C. fecunda, are sympatric. These species are morphologically cryptic and differ only in their larval development: C. dilatata has indirect development with a planktonic phase, and C. fecunda direct development within egg capsules. The other two species, C. coquimbensis and C. philippiana, are species that occur within gastropod shells inhabited by hermit crabs and differ from the other species in internal morphology of the shell, developmental features, and geographic distribution. Analyses of nine morphological characters, eight developmental characters, and 26 enzymatic loci were carried out on four Crepidula populations in the Coquimbo region of northern Chile. Four populations of Crepidula were identified based on morphological, developmental, and protein electrophoresis features. Our results suggest the presence of C. coquimbensis plus three morphologically cryptic species including C. dilatata, C. fecunda, and a new previously unrecognized cryptic species. All four populations showed differences in larval development pattern. C. fecunda have indirect development, with free-swimming larvae. The remaining three species have intracapsular metamorphosis, but different modes of larval nutrition. C. dilatata have nurse eggs that are consumed by mechanical destruction; C. coquimbensis engulf nutritional embryos; and the new species eat nutritive embryos by rotation. Protein electrophoresis data support the specific condition of each group with different larval development and endorse the use of developmental differences in taxonomy of Crepidula. Genetic distance shows that C. dilatata and C. fecunda are closely related, and that C. coquimbensis is closer to them than to the new cryptic species.

What can DNA Tell us About the Cambrian Explosion?

Molecular data is ideal for exploring deep evolutionary history because of its universality, stochasticity and abundance. These features provide a means of exploring the evolutionary history of all organisms (including those that do not tend to leave fossils), independently of morphological evolution, and within a statistical framework that allows testing of evolutionary hypotheses. In particular, molecular data have an important role to play in examining hypotheses concerning the tempo and mode of evolution of animal body plans. Examples are given where molecular phylogenies have led to a re-examination of some fundamental assumptions in metazoan evolution, such as the immutability of early developmental characters, and the evolvability of bauplan characters. Molecular data is also providing a new and controversial timescale for the evolution of animal phyla, pushing the major divisions of the animal kingdom deep into the Precambrian. There have been many reasons to question the accuracy and precision of molecular date estimates, such as the failure to account for lineage-specific rate variation and unreliable estimation of rates of molecular evolution. While these criticisms have been largely countered by recent studies, one problem has remained a challenge: could temporal variation in the rate of molecular evolution, perhaps associated with "explosive" adaptive radiations, cause overestimation of diversification dates? Empirical evidence for an effect of speciation rate, morphological evolution or ecological diversification on rates of molecular evolution is examined, and the potential for rate-variable methods for molecular dating are discussed.

Worldwide patterns in mode of development in calyptraeid gastropods

The mode of development in marine invertebrates is believed to have consequences for dispersal, gene flow, geographic range, and speciation and extinction rates. The factors responsible for among-species differences in mode of development are not well understood and patterns of vari- ation in mode of development have not been documented for many groups. I present a compiled data set of developmental characters for 78 species of calyptraeid gastropods: 53 Crepidula, 9 Calyptraea, 11 Crucibulum and 5 other species. Analysis of this data set shows that egg- and hatching-size distri- butions are strongly positively skewed. As expected, egg size correlates with hatching size and time to hatching in species without nurse eggs. Egg size is not significantly different between species with planktotrophic development and species with direct development with nurse eggs. Hatching size of direct developers with and without nurse eggs do not differ. Developmental characters do not vary with adult body size among species. There are strong latitudinal effects in mode of development, the frequency of planktotrophic species decreases with increasing latitude while the proportion of direct developers increases. There is also a striking latitudinal pattern in the occurrence of nurse eggs; almost all species with nurse eggs occur in the southern hemisphere. These latitudinal patterns do not appear to be explained by sea surface temperature. Comparisons with other gastropods for which similar compilations are available show a striking difference between heterobranchs (opisthobranchs and pulmonates) and caenogastropods in developmental characteristics.

New directions in comparative embryology and the nature of developmental characters

AbstractDoes developmental anatomy have a future in the age of molecular biology and digital technologies? Specifically, will morphological characters continue to be used in comparative developmental biology, or will new types of character be defined? Traditionally, comparative embryology was a non-quantitative, 'portrait-gallery' science. Wilhelm His attempted to develop a character-based, more quantitative approach. Quantitative approaches to development have been also been suggested by Meinhardt and others. With the current availability of computing power and the growth of bioinformatics and phylogenetic methodology, quantitative methodologies are increasingly being applied to studies of embryonic development. Our aim in this article is to examine some of these approaches. In both anatomical and molecular studies, the parameters to be quantified are temporal and spatial. Temporal data are analysed by techniques, such as event pairing, that analyse developmental sequences. In this case, the characters are developmental events. Spatial information can be analysed using morphometrics, in combination with computer-assisted 3D reconstruction. In spatial analyses, anatomical parts may be used as the characters. A major challenge in the coming years is to develop techniques for analysing 3D patterns of developmental gene expression and to compare them between species or individuals. Such analyses have to be defined in relation to five dimensions: the 3 orthogonal spatial planes; time; and individuals. The difficulties of such analyses are complicated by problems of homology. Some possible solutions are suggested. For example, it may be possible to use voxels as characters, and to assign to them attributes according to gene expression domains. At first sight, it might seem that traditional morphological characters would no longer be required in comparative embryology. However, we believe that some kind of anatomical framework will always be needed in comparative biology. The interplay between classical morphological characters, gene expression patterns and computing methodologies will be an exciting area for future work.

Inflorescence diversification in the panicoid “bristle grass” clade (Paniceae, Poaceae): evidence from molecular phylogenies and developmental morphology

Grasses exhibit a great variety of inflorescence forms and these appear homoplasious when mapped onto cladograms. The overall pattern is sufficiently complex that it is difficult to analyze inflorescence evolution. We have reduced the complexity of the problem by examining one group of grasses, the panicoid "bristle clade," which exhibits a less complex pattern of variation. The clade is morphologically defined by inflorescences bearing both spikelets and sterile bristles and is monophyletic in both morphological and molecular phylogenetic analyses. We have constructed a chloroplast DNA phylogeny of the three main genera, which finds three well-supported clades, two comprising species placed in Setaria and one of Pennisetum + Cenchrus. In this tree Cenchrus is monophyletic, but both Setaria and Pennisetum are paraphyletic. Developmental morphology of these groups is very similar at early stages. Changes in axis ramification, primordial differentiation, and axis elongation account for most variation in mature inflorescence morphology. Characters derived from comparisons of developmental sequences were optimized onto one of the most parsimonious trees. Most developmental characters were congruent with the molecular phylogeny except for three reversals in the subclade containing S. barbata, S. palmifolia, and two accessions of S. poiretiana. Changes in just a handful of developmental events account for inflorescence evolution in the bristle clade, and similar changes may account for inflorescence diversity in the grasses as a whole.

Phylogeny of Stemphylium spp. Based on ITS and Glyceraldehyde-3-Phosphate Dehydrogenase Gene Sequences

The phylogenetic relationships among 44 isolates representing 16 species of Stemphylium were inferred from ITS and glyceraldehyde-3-phosphate dehydrogenase (gpd) sequence data. The results generally agree with morphological species concepts. There was strong support for monophyly of the genus Stemphylium. Analysis of the gpd fragment in particular was useful for establishing well-supported relationships among the species and isolates of Stemphylium. Species of Stemphylium that appear to have lost the ability to produce a sexual state are scattered among the species with the ability to reproduce sexually (Pleospora spp.). Species that are pathogenic to alfalfa are resolved into two groups. Stemphylium botryosum and two isolates with morphological characters similar to S. globuliferum had identical sequences at both loci. These two loci in S. vesicarium, S. alfalfae and S. herbarum are nearly identical but differ from S. botryosum. The separation of S. vesicarium, S. herbarum and S. alfalfae into separate species by morphometric evidence was not supported by the molecular data. Morphological and developmental characters such as size and shape of conidia, conidiophores, and ascospores, and size and time of maturation of pseudothecia are useful for diagnosing species. However, other morphological characters such as septum development and small variations in conidial wall ornamentation are not as useful.

Phylogeny of Stemphylium spp. based on ITS and glyceraldehyde-3-phosphate dehydrogenase gene sequences

The phylogenetic relationships among 44 isolates representing 16 species of Stemphylium were inferred from ITS and glyceraldehyde-3-phosphate dehydrogenase (gpd) sequence data. The results generally agree with morphological species concepts. There was strong support for monophyly of the genus Stemphylium. Analysis of the gpd fragment in particular was useful for establishing well-supported relationships among the species and isolates of Stemphylium. Species of Stemphylium that appear to have lost the ability to produce a sexual state are scattered among the species with the ability to reproduce sexually (Pleospora spp.). Species that are pathogenic to alfalfa are resolved into two groups. Stemphylium botryosum and two isolates with morphological characters similar to S. globuliferum had identical sequences at both loci. These two loci in S. vesicarium, S. alfalfae and S. herbarum are nearly identical but differ from S. botryosum. The separation of S. vesicarium, S. herbarum and S. alfalfae into separate species by morphometric evidence was not supported by the molecular data. Morphological and developmental characters such as size and shape of conidia, conidiophores, and ascospores, and size and time of maturation of pseudothecia are useful for diagnosing species. However, other morphological characters such as septum development and small variations in conidial wall ornamentation are not as useful.

The terminology of larval cestodes or metacestodes

The terminology associated with the nomenclature of larval or metacestodes is reviewed as well as the various morphological and developmental characters used to define different types of larval cestodes. Based on a review of the literature, the key characters differentiating the types of larval cestodes are the presence of a primary lacuna and the invagination/retraction of the scolex. The presence of a cercomer and of a bladder-like enlargement of the larval cestode were considered to be useful secondary characteristics. Using these characters, six basic types of larval cestodes were identified: the procercoid, an alacunate form which cannot develop further until ingested by a second intermediate host; the plerocercus, an alacunate form with a retracted scolex; the plerocercoid, an alacunate form with an everted scolex; the merocercoid, an alacunate form with an invaginated scolex; the cysticercoid, a lacunate form with a retracted scolex; and the cysticercus, a lacunate form with an invaginated scolex. The diversity of larval types within the broad classifications of cysticercoid and cysticercus can be differentiated by the use of appropriate prefixes. Deficiencies in knowledge of specific types of larval cestodes are identified and further avenues of research are indicated.

Present status and future of nematode systematics

AbstractSince phylogenetic systematics became generally accepted and especially since informatics and molecular techniques for phylogenetic analysis were developed, systematics has undergone a conceptual and methodological revolution. Taxonomy, on the contrary, suffered a decline. Poor descriptions, too much routine work and low citation rates hampered it. As a result, the discipline became less attractive to young scientists. With only a small fraction of the biodiversity known, this situation will lead to serious problems in the future in all those fields of nematology depending on a correct identification of species. Phylogenetic analyses of nematodes have been mainly based on morphology, supplemented with developmental characters, but in recent years molecular methods have provided entirely new data sets. Phylogenetic estimates derived from independent data may provide new insights in character homologies through reciprocal illumination. Classifications of nematodes were often biased according to the expertise of the author and were only recently based on the principles of phylogenetic systematics. Recently, molecular and morphological data have been used to support a new overall classification with only (presumably) monophyletic taxa. In this classification plant, as well as animal, parasitic taxa are hierarchically downgraded in accordance with their phylogenetic history. Species occupy an important position in all aspects of biology, therefore the species concept matters. It determines, for example, the outcome of biodiversity assessments, distribution patterns, etc. However, several problems remain to be solved before a consensus will be reached about the choice of a concept. Future research in nematode systematics should comprise well-focused taxonomy based on a combination of classical and modern methods in a way that can raise the interest of young scientists as well as of funding agencies. It should be realised that, with the dwindling present taxonomic expertise, this is a very urgent matter.

CELL LINEAGE DATA AND SPIRALIAN EVOLUTION: A REPLY TO NIELSEN AND MEIER

CELL LINEAGE DATA AND SPIRALIAN EVOLUTION: A REPLY TO NIELSEN AND MEIER

Molecular data indicate the protostome affinity of brachiopods.

Although the phylogenetic position of brachiopods has always been subject to debate, many authors place them as a sister group to deuterostomes on the basis of morphological and developmental characters. However, molecular phylogeny consistently places them among protostomes. More precisely, brachiopods are predicted to branch inside the lophotrochozoan assemblage, together with annelids, molluscs, nemerteans, flatworms, and others. That result has been criticized on the basis of (1) prior knowledge of brachiopod morphology and (2) the known limitations of molecular phylogenies. Here I review recent data of molecular origin, particularly those displaying qualitative properties close to those of morphological characters. The complement of Hox genes present in all metazoa tested to date has proved to be a powerful tool for broad phylogenetic reconstruction. The mitochondrial genome also provides qualitative characters, showing discrete events of gene rearrangements. After discussing the data and the way they should be interpreted in the perspective of several hypotheses for metazoan phylogeny, I conclude that they argue strongly in favor of the protostome (and lophotrochozoan) affinity of the brachiopods. There is therefore a need for a reinterpretation of brachiopod morphological and developmental characters. I also identify some research axes on brachiopod morphology.

Character coding of secondary chemical variation for use in phylogenetic analyses.

A coding procedure is presented for secondary chemical data whereby putative biogenetic pathways are coded as phylogenetic characters with enzymatic conversions between compounds representing the corresponding character states. A character state tree or stepmatrix allows direct representation of the secondary chemical biogenetic pathway and avoids problems of non-independence associated with coding schemes that score presence/absence of individual compounds. Stepmatrices are the most biosynthetically realistic character definitions because individual and population level polymorphisms can be scored, reticulate enzymatic conversions within pathways may be represented, and down-weighting of pathway loss versus gain is possible. The stepmatrix approach unifies analyses of secondary chemicals, allozymes, and developmental characters because the biological unity of the pathway, locus, or character ontogeny is preserved. Empirical investigation of the stepmatrix and character state tree coding methods using floral fragrance data in Cypripedium (Orchidaceae) resulted in cladistic relationships which were largely congruent with those suggested from recent DNA and allozyme studies. This character coding methodology provides an effective means for including secondary compound data in total evidence studies. Furthermore, ancestral state reconstructions provide a phylogenetic context within which biochemical pathway evolution may be studied.

Intraspecific Variation in Developmental Characters: The Origin of Evolutionary Novelties

Intraspecific Variation in Developmental Characters: The Origin of Evolutionary Novelties

Intraspecific Variation in Developmental Characters: The Origin of Evolutionary Novelties1

Abstract Evolutionary developmental biology is inevitably a comparative subject. However, the taxonomic level at which comparisons can be made varies widely, and this greatly affects the kind of information that can be gained from the comparison. Broadly speaking, high-level comparisons (e.g., between phyla) are more informative about phylogenetic pattern and homology, while low-level comparisons (e.g., between congeneric species) are more informative about evolutionary mechanisms, including speciation. However, so far evolutionary developmental biology has had a relatively minor input into the traditional territory of population genetics, namely comparisons within species—both within and between geographic populations. Yet this area is crucial, as all evolutionary novelties ultimately arise from intraspecific variation. Here, I address this issue, focusing on the question of how early in development novelties arise. To shed light on this question, I discuss two examples of developmental polymorphism with...

Dispersal behaviour in a subsocial spider: group conflict and the effect of food availability

This study investigates proximate factors influencing dispersal behaviour in the subsocial spider Amaurobius ferox. Dispersal of spiderlings from the natal web occurred as a progressive sigmoidal function (mean duration of dispersal period=31 days), with considerable individual variability in developmental instar and body mass within the clutch at the time of dispersal. The spiderlings showed a significant decrease in group cohesion on the 6th day after their second moult, which corresponded to the beginning of the dispersal period. Mutual aggressiveness appeared when the spiderlings began to show predatory behaviour (4th day post-second moult) and increased over the course of the dispersal period. While lack of prey in the maternal nest accelerated dispersal behaviour, the addition of prey items lengthened the dispersal period in previously non-fed clutches. Individuals that dispersed were smaller than the remaining individuals when measured on the day 50% of the clutch had dispersed. Timing of the appearance of the developmental characters (second moult, predation activity, agonistic behaviour against siblings, reduction of group cohesion, dispersal) suggests that the dispersal trait might have evolved in consequence of these different functional behaviours.

Opercular development and ontogenetic re-organization in a direct-developing frog.

The direct-developing frog, Eleutherodactylus coqui, has eliminated the tadpole stage from its ontogeny, and lacks many larval characters. We demonstrate that the dermal folds of E. coqui are homologous with the opercular folds of metamorphosing frogs. In both E. coqui and its metamorphic counterparts the opercular folds grow over the developing forelimb before perforating to free the entrapped limb. Opercular perforation in E. coqui occurs even in the absence of the forelimb but shows no signs of thyroid hormone dependence. The condensation of E. coqui development appears due to the excision of the extended larval period of developmental stasis. Analysis of opercular development, when viewed in conjunction with other developmental characters, suggests the ontogenetic period in the ancestral Eleutherodactylus life-history from which the tadpole was likely eliminated.

Convergent adaptive radiations in Madagascan and Asian ranid frogs reveal covariation between larval and adult traits.

Recent studies have reported that independent adaptive radiations can lead to identical ecomorphs. Our phylogenetic analyses of nuclear and mitochondrial DNA sequences here indicate that a major radiation of ranid frogs on Madagascar produced morphological, physiological, and developmental characters that are remarkably similar to those that independently evolved on the Indian subcontinent. We demonstrate further that, in several cases, adult and larval stages each evolved sets of characters which are not only convergent between independent lineages, but also allowed both developmental stages to invade the same adaptive zone. It is likely that such covariations are produced by similar selective pressures on independent larval and adult characters rather than by genetic or functional linkage. We briefly discuss why larval/adult covariations might constitute an important evolutionary phenomenon in species for which more than one developmental stage potentially has access to multiple environmental conditions.

Genetic variance of sexually selected traits in waxmoths: maintenance by genotype x environment interaction.

When traits experience directional selection, such as that imposed by sexual selection, their genetic variance is expected to diminish. Nonetheless, theory and findings from sexual selection predict and demonstrate that male traits favored by female choice retain substantial amounts of additive genetic variance. We explored this dilemma through an ecological genetic approach and focused on the potential contributions of genotype x environment interaction (GEI) to maintenance of additive genetic variance for male signal characters in the lesser waxmoth, Achroia grisella (Lepidoptera: Pyralidae). We artificially selected genetic variants for two male signal characters, signal rate (SR) and peak amplitude (PA), that influence female attraction and then examined the phenotypic plasticity of these variants (high- and low-SR and high- and low-PA lines) under a range of environmental conditions expected in natural populations. Our split-family breeding experiments indicated that two signal characters, SR and PA, and several developmental characters in both high- and low-SR and high- and low-PA lines displayed considerable phenotypic plasticity among the environments tested. Moreover, strong GEIs leading to crossover between high- and low-SR lines were found for SR and developmental period. Therefore, neither high- nor low-SR genetic variants would achieve maximum attractiveness and fitness in every environment, and those variants producing unattractive signals with low SRs under normal conditions may remain in populations provided that gene flow across environments or generation overlap are sufficiently high. We speculate that the phenotypic plasticity for SR and developmental period is adaptive in A. grisella populations experiencing a range of temperature and density conditions. Females mating with attractive (high-SR) males may be assured of obtaining good genes because these males sire offspring that develop more rapidly and a crossover for developmental period may parallel that for SR. Such parallel crossovers may be expected wherever good-genes sexual selection mechanisms operate.

Arthropod Cladistics: Combined Analysis of Histone H3 and U2 snRNA Sequences and Morphology

Morphological, developmental, ultrastructural, and gene order characters are catalogued for the same set of arthropod terminals as we have scored in a recent study of histone H3 and U2 snRNA sequences (D. J. Colgan et al., 1998, Aust. J. Zool. 46, 419–437). We examine the implications of separate and simultaneous analyses of sequence and non-sequence data for arthropod relationships. The most parsimonious trees based on 211 non-sequence characters (273 apomorphic states) support traditional higher taxa as clades, including Mandibulata, Crustacea, Atelocerata, Myriapoda, and Hexapoda. Combined analysis of morphology with histone H3 and U2 sequences with equal character weights differs from the morphological results alone in supporting Progoneata + Hexapoda (= Labiophora) in favor of a monophyletic Myriapoda, resolves the entognathous hexapods as a grade, and supports pycnogonids as sister group to Euchelicerata (rather than as basal euarthropods). Monophyly of Chelicerata (including pycnogonids), Mandibulata, Crustacea, Progoneata, Chilopoda, and Hexapoda is maintained under a range of transition/transversion and third codon weights, whereas Atelocerata and Myriapoda/Labiophora do not withstand all sensitivity analyses.