Floral ontogenetic evidence of repeated speciation via paedomorphosis in subtribe Orchidinae (Orchidaceae)

Thoroughly sampled molecular phylogenies of the dominantly European orchid subtribe Orchidinae were used to identify a pair and a triplet of recently diverged species in which: (1) divergence involved substantial changes in floral morphology, particularly in the labellar lobes and spur; and (2) the polarity of those changes could be inferred phylogenetically. Floral ontogeny in the selected species was documented in detail through macromorphological, light microscopic, and scanning electron microscopic study of a wide range of ontogenetic stages. All study species showed differentiation of perianth segments earlier than the gynostemium. Unsurprisingly, component parts of the basic floral organs (gymnostemial auricles and rostellum, labellar lateral lobes, and spur) were initiated relatively late, the spur and ovary continuing to expand beyond anthesis. The predominant evolutionary pattern identified in the two case studies was paedomorphosis via progenesis (earlier offset of growth); this credibly explained the reduction in spur size and lateral lobing of the labellum in Gymnadenia odoratissima and, especially, G. austriaca relative to G. conopsea. Loss of resupination in G. austriaca was best viewed as the deletion of a formerly terminal ontogenetic stage. Radical reduction of the spur of Dactylorhiza viridis relative to D. fuchsii was also attributed to progenesis, although the long, narrow outline and relatively short central lobe of its labellum were attributed to increased growth of the lateral lobes (i.e. hypermorphosis resulting in peramorphosis). Microscopic study of epidermal cell types on the labellum and spur suggested a degree of decoupling of micromorphological from macromorphological transitions, although both were subject to heterochronic shifts. Each of the two case studies was consistent with, but not proof of, saltational macroevolution operating via functional changes in one or more key developmental genes. © 2008 The Linnean Society of London, Botanical Journal of the Linnean Society, 2008, 157 , 429–454.     

Timing of epiphyseal development in the flipper skeleton of the harbour porpoise (Phocoena phocoena) as an indicator of paedomorphosis

Epiphyseal development was investigated on X‐rays of flippers from 158 harbour porpoises from Danish waters. Development followed a proximodistal pattern similar to what is known in other cetacean species. Ossification of epiphyses was rare in the phalanges of the first and fifth digits and in the more distal phalanges of the second, third and fourth digits. Along with the morphology of the first metacarpal and the more distal phalanges this suggested paedomorphosis relative to delphinids. Male and female porpoises showed similar progression of epiphyseal development until approximately the sixth year. From then on, female porpoises showed more progressed development than males. This suggests a higher level of paedomorphosis in the male porpoise. The mechanism behind phocoenid paedomorphosis seems to be progenesis, probably as an adaptation towards a high reproductive rate relative to the delphinids.     

Molecular phylogenetic perspective on the evolution of the deep-sea fish genusCyclothone (Stomiiformes: Gonostomatidae)

A portion of mitochondrially encoded 12S and 16S ribosomal RNA genes were sequenced from 13 currently recognized species of the midwater deep-sea fish genusCyclothone (Stomiiformes: Gonostomatidae) and three gonostomatid outgroup taxa. Phylogenetic analyses using maximum parsimony and maximum likelihood methods were performed on unambiguously aligned, combined sequences (803 bp) of the two genes. The resultant tree topologies from the two methods were congruent, being robust and supported by various tree statistics, enabling the evolutionary history ofCyclothone to be described in detail. The molecular phylogeny demonstrated striking inconsistencies with previously proposed “natural groups”, although the latter could be confidently refuted by the molecular data. The most significant characteristic of the evolutionary history ofCyclothone was the independent acquisition of an apomorphic depth habitat from the relatively ancestral, lower mesopelagic habitat, by each of three major distinct lineages that had diverged earlier in their evolution. Moreover, such macroevolutionary habitat shifts had been necessarily accompanied by morphological and ecological novelties, presumably originating from paedomorphosis. Repeated evolution of such changes strongly suggests ontogenetic plasticity inCyclothone which could enable these fishes to acquire larval-like, simple organization of body structure. Such a body plan could help them subsist in food-poor surroundings and regulate reproductive variables that take advantage of increasing larval survival toward shallower depths. Recent speciation events, on the contrary, have produced contemporary sister species of allopatric (or microallopatric) distributions, but few morphological and ecological differences. Even if remarkable miniaturization has occurred, such as in the Mediterranean endemicC. pygmaea, it had to have been a simple truncation of ancestral species' ontogeny without attendance of any discernible paedomorphic features. On the basis of the fossil record, geological history of the Mediterranean region, and ectotherm molecular divergence rate, it was estimated thatCyclothone radiation had already started in the early-middle Miocene (17–20 million years ago).     

Evolution of the self-pollinating flower in Clarkia xantiana (Onagraceae). I. Size and development of floral organs

Clarkia xantiana has two subspecies that differ in breeding system: ssp. xantiana, which is outcrossing, and ssp. parviflora, which is self-fertilizing. Outcrossing is the ancestral breeding system for the genus Clarkia. Flowers of ssp. parviflora have characteristics commonly associated with selfing taxa: they are smaller and have little temporal and spatial separation between mature anthers and stigma (dichogamy and herkogamy, respectively). Flower morphology and development were studied in four populations of each subspecies to establish the developmental changes that occurred in the evolution of selfing. In particular, we sought to evaluate the hypothesis that the selfing flower may have arisen as a byproduct of selection for rapid maturation in the arid environment occupied by ssp. parviflora. This hypothesis predicts that development time should be reduced in spp. parviflora relative to ssp. xantiana. We also sought to compare the pattern of covariation of flower morphology and development between subspecies to that within subspecies. Similar within vs. between patterns of covariation could be indicative of developmental or functional constraints on the independent evolution of floral parts. In spite of significant variation among populations within subspecies, the subspecies clearly differ in flower morphology and development. All floral organs, except ovaries, are smaller in ssp. parviflora than in ssp. xantiana. The flower plastochron, the duration of flower development from bud initiation to anthesis, and the duration of protandry are all shorter in ssp. parviflora than in ssp. xantiana. Maximum relative growth rates are higher for all organs in ssp. parviflora than in ssp. xantiana. Thus, progenesis (i.e., via a reduction in development time) is combined with growth acceleration in the evolution of the selfing flower. Since reduced development time and growth acceleration both allow selfing flowers to mature earlier than outcrossing ones, selection for early maturation may have contributed to the evolution of the selfing flower form. The pattern of trait covariation differs within spp. parviflora relative to the patterns within spp. xantiana and between the two subspecies, suggesting that floral parts can and have evolved independently of one another.     

Morphological novelty and modest developmental truncation in Barboides,Africa's smallest vertebrates (Teleostei: Cyprinidae)

Miniaturization, the evolution of extremely small adult body size, is widespread amongst animals and commonly associated with novel ecological, physiological, and morphological attributes. The phenotypes of miniaturized taxa are noteworthy because they combine reductions and structural simplifications with novel traits not developed in their larger relatives. Previous research on miniature cyprinid fishes (focused predominantly on South and South East Asian taxa of a single subfamily) has identified two distinct classes of miniature taxa: proportioned dwarves and developmentally truncated miniatures. Miniaturization has also occurred independently in the subfamily Cyprininae, particularly in African lineages. We investigate the skeletal anatomy of Barboides , a genus of miniature African cyprinids that includes Africa's smallest known species of vertebrates, to assess whether miniaturization has resulted in similar organismal outcomes in different lineages of the Cyprinidae. The skeleton of Barboides is characterized by the complete absence of a number of dermal and endochondral ossifications, and marked reduction in size and/or complexity of other skeletal elements, particularly those of the dermatocranium. Absent skeletal elements in Barboides include those which develop relatively late in the ossification sequence of the non‐miniature African relative ‘Barbus ’ holotaenia suggesting that their absence in Barboides can be explained by a simple scenario of developmental truncation. In contrast to this theme of loss and reduction, the os suspensorium of Barboides is enlarged and the outer arm distally trifid and associated with a novel bulbous muscle in males. An evaluation of the skeleton of Barboides provides further evidence for a link between developmental truncation and evolutionary morphological novelty in Cyprinidae. In the spectrum of miniature cyprinids ranging from proportioned dwarves with few bones missing to highly progenetic taxa with dozens of missing bones, the two species of Barboides range roughly in the middle showing that the extremes are connected by intermediate levels of truncatedness.     

Life cycle abbreviation in the trematode Coitocaecum parvum: can parasites adjust to variable conditions?

The complex life cycles of parasites are thought to have evolved from simple one-host cycles by incorporating new hosts. Nevertheless, complex developmental routes present parasites with a sequence of highly unlikely transmission events in order to complete their life cycles. Some trematodes like Coitocaecum parvum use facultative life cycle abbreviation to counter the odds of trophic transmission to the definitive host. Parasites adopting life cycle truncation possess the ability to reproduce within their intermediate host, using progenesis, without the need to reach the definitive host. Usually, both abbreviated and normal life cycles are observed in the same population of parasites. Here, we demonstrate experimentally that C. parvum can modulate its development in its amphipod intermediate host and adopt either the abbreviated or the normal life cycle depending on current transmission opportunities or the degree of intra-host competition among individual parasites. In the presence of cues from its predatory definitive host, the parasite is significantly less likely to adopt progenesis than in the absence of such cues. An intermediate response is obtained when the parasites are exposed to cues from non-host predators. The adoption of progenesis is less likely, however, when two parasites share the resource-limited intermediate host. These results show that parasites with complex developmental routes have transmission strategies and perception abilities that are more sophisticated than previously thought.     

Architecture of the nervous system in mystacocarida (Arthropoda,crustacea)—An immunohistochemical study and 3D reconstruction

Mystacocarida is a species‐poor group of minute crustaceans with unclear phylogenetic affinities. Previous studies have highlighted the putative “primitiveness” of several mystacocarid features, including the architecture of the nervous system. Recent studies on arthropod neuroarchitecture have provided a wealth of characters valuable for phylogenetic reconstructions. To permit and facilitate comparison with these data, we used immunohistochemical labeling (against acetylated α‐tubulin, serotonin and FMRFamide) on the mystacocarid Derocheilocaris remanei, analyzing it with confocal laser‐scanning microscopy and 3D reconstruction. The mystacocarid brain is fairly elongated, exhibiting a complicated stereotypic arrangement of neurite bundles. However, none of the applied markers provided evidence of structured neuropils such as a central body or olfactory glomeruli. A completely fused subesophageal ganglion is not present, all segmental soma clusters of the respective neuromeres still being delimitable. The distinct mandibular commissure comprises neurite bundles from more anterior regions, leading us to propose that it may have fused with an ancestral posterior tritocerebral commissure. The postcephalic ventral nervous system displays a typical ladder‐like structure with separated ganglia which bears some resemblance to larval stages in other crustaceans. Ganglia and commissures are also present in the first three limbless “abdominal” segments, which casts doubt on the notion of a clear‐cut distinction between thorax and abdomen. An unpaired longitudinal median neurite bundle is present and discussed as a potential tetraconate autapomorphy. Additionally, a paired latero‐longitudinal neurite bundle extends along the trunk. It is connected to the intersegmental nerves and most likely fulfils neurohemal functions. We report the complete absence of serotonin‐ir neurons in the ventral nervous system, which is a unique condition in arthropods and herein interpreted as a derived character. J. Morphol., 2010. © 2009 Wiley‐Liss, Inc.     

The genetic control of heterochrony: Evidence from developmental mutants of Pisum sativum L.

Heterochrony, as a means of evolution in which the rate or timing of developmental events of the descendant is altered compared with that of the ancestor, is of significance because it suggests that rapid and dramatic morphological changes are possible with few genetic changes. The putative origin of plant taxa by this means of evolution is becoming increasingly frequent in the literature but there is little evidence of the extent of the genetic change necessary to alter the timing of developmental events to produce such changes. This study shows that the onset of flowering can be altered independently from the vegetative transition in leaf form in at least one genotype of Pisum in response to different environments. Further, it identifies 9 mutations that act in a heterochronic manner to produce dramatic morphological changes that can be described as progenesis, neoteny, hypermorphosis or acceleration. In addition, it is demonstrated that the same heterochronic process (e.g. progenesis) may be caused by genes controlling distinctly different physiological processes. It is suggested that Pisum is an ideal model species for studies of heterochrony and that few genetic changes are necessary to bring about dramatic heterochronic changes.     

Progenesis in dicyemids

Dicyemids (Phylum Dicyemida) are the most common and characteristic endosymbiont living in the renal sac of benthic cephalopod molluscs. Precocious development of a hermaphroditic gonad occurs in the larvae and smaller juveniles of 40 dicyemid species from 17 cephalopod species so far and is the usual phenomenon in dicyemids. Based on the developmental and morphological features of precocious individuals, progenesis (a form of heterochrony) is the appropriate term for such precocious development. In general, progenetic individuals have much lower fecundity than normal ones because of their smaller body size, and therefore, it appears to be a disadvantageous reproductive trait. Nonetheless, the number of progenetic individuals consists of 30%–50% of the population, a relatively large proportion suggesting that the presence of progenetic individuals probably plays an important role in life history strategy. Precocious development significantly reduces growth time and enables early maturation. Progenetic individuals are common in short-living cephalopod species, in which precocious development seems appropriate for dicyemids, enabling fast larval release before the end of the host's life span.