Reinterpreting recapitulation: systematics of needlefishes and their allies (Teleostei: Beloniformes)

Abstract. As needlefishes (Belonidae) grow, their jaws pass through a "halfbeak" stage that resembles the adult jaw condition of the closely related family of halfbeaks (Hemiramphidae). Based on this pattern, some authors have suggested that halfbeaks are "developmentally arrested" or paedomorphic needlefish derivatives, whereas others have supported the notion that needlefishes are descended from halfbeak-like ancestors and that needlefish ontogeny thereby recapitulates phylogeny. To test these ideas and to better understand evolutionary changes in jaw ontogeny, phylogenetic relationships among genera of needlefishes, sauries (Scomberesocidae), halfbeaks, and flyingfishes (Exocoetidae) were assessed using mitochondrial (cytochrome b and 16S), nuclear (Tmo-4C4), and morphological characters. The resultant tree provides several novel taxonomic findings: (1) flyingfishes appear to be nested within halfbeaks; (2) sauries appear to be nested within needlefishes; and (3) the Indo-West Pacific freshwater halfbeaks appear to be most closely related to the needlefish/saury clade. The structure of the tree falsifies the idea that halfbeaks are paedomorphic needlefishes. Instead, halfbeaks are basal relative to needlefishes, fitting the pattern predicted by the hypothesis of recapitulation. I discuss limitations to phylogenetic perspectives on recapitulation based on discrete character data by comparing aspects of von Baerian and Haeckelian views of the relation between ontogeny and phylogeny.     

Modifications of the falciform process in the eye of beloniformes (Teleostei: Atherinomorpha): evolution of a curtain-like septum in the eye

In order to comparatively analyze curtain-like septa in the eyes of visually orientated "close-to-surface-predators" among atherinomorph teleosts, we examined the eyes of 24 atherinomorph species under a binocular microscope with regard to the falciform process and related structures in the vitreous cavity. Additionally, falciform process samples were analyzed by transmission electron microscopy. All the studied representatives of the Cyprinodontiformes and Atheriniformes, and of one of the beloniform suborder, Adrianichthyioidei, possess a "typical" processus falciformis. In the eyes of the representatives of the other beloniform suborder, Belonoidei, however, pigmented structures that originate in the region of the optic disc and protrude into the vitreous cavity were noted. In the Hemiramphidae (halfbeaks) and Exocoetidae (flying fishes) these pigmented structures have a more cone-like shape, whereas in the Belonidae (needlefishes) and Scomberesocidae (sauries) horizontally oriented heavily pigmented curtain-like septa occur that divide the vitreous cavity dorsoventrally. It is suggested that the "typical" processus falciformis represents a plesiomorphic feature within the Atherinomorpha, whereas the pigmented modifications of the falciform process must be seen as a synapomorphic character state of the Belonoidei. The curtain-like septum of the Belonidae and Scomberesocidae might have evolved from the cone-like structures that are found in the Exocoetoidea. The functional significance of the pigmented structures in the eye is as yet not clear, except for the curtain-like septum found in Belonidae. It might play a role in visual orientation near the water surface at Snell's window.     

Enzymatic digestion in stomachless fishes: how a simple gut accommodates both herbivory and carnivory

The lack of a stomach is not uncommon amongst teleost fishes, yet our understanding of this reductive specialisation is lacking. The absence of a stomach does not restrict trophic preference, resulting in fishes with very similar alimentary morphology capable of digesting differing diets. We examined the digestive biochemistry of four beloniform fishes: two herbivorous halfbeaks (Hemiramphidae) and two carnivorous needlefish (Belonidae) to determine how these fishes digest their respective diets with their simple, short gut. We found that although the halfbeaks showed significantly greater α-amylase activity than that of the needlefish (P < 0.01), trypsin, lipase, aminopeptidase and maltase activity were not substantially different between the two families. We also found that habitat (freshwater vs. marine) appears to play a significant role in digestive capability, as the two freshwater taxa and the two marine taxa were significantly different (ANOSIM; dietary Gobal R = 0.544, P = 0.001, habitat Global R = 0.437, P = 0.001), despite their phyletic and dietary similarities. Our findings offer partial support for the adaptive modulation hypothesis, support the Plug-Flow Reactor model of digestion in herbivorous halfbeaks and also support the compartmental model of digestion but suggest that another model is required to describe stomachless carnivorous needlefish.     

Ontogeny–a way forward for systematics, a way backward for phylogeny

In the history of biology, the term 'evolution' has carried a dual meaning, viz. ontogeny (the unfolding of the germ) versus phylogeny (descent with modification). A problem in modern biology is the question of whether it is ontogeny which creates phylogeny, or whether it is phylogeny which moulds ontogeny. The paper explores the relationship of ontogeny to phylogeny in the context of 'pattern cladism'. The conclusion is that the analysis of ontogeny provides a direct method for classification ('a way forward for systematics'), which is a logical prerequisite for a phylogenetic interpretation of ontogenetic sequences ('a way backward for phylogeny'). The ontogenetic process of growth, subdivision and differentiation is related to the 'morphogenetic tree theory' on the basis of Von Baer's "laws of individual development". This conceptual relation shows that ontogeny creates phylogeny in an upward direction within the morphogenetic tree, whereas phylogeny (by means of natural selection) moulds ontogeny in a downward direction. A conflict originates with the conventions of Linnaean classification if ontogenetic divergence is proposed as a causal agent in the origin of higher taxa. It is proposed to solve this conflict by viewing individual organisms (or reproductive communities) not as constituents, but as representatives of higher taxa.     

ONTOGENY AND THE HIERARCHY OF TYPES

Abstract— The long history of belief in a parallelism between ontogeny and a hierarchical order of natural things is reviewed. The meaning of von Baerian recapitulation is analyzed and its implications for cladistic methodology are discussed at two levels: ontogeny and homology. The basic problem inherent in the purported parallelism is that the order of natural things (i.e., the taxic approach to homology) is part of the "world of being" of Platonic ideas, whereas ontogeny and phylogeny (i.e., the transformational approach to homology) belong to Plato's "world of becoming." These two "genera of existence," as Plato put it, being and becoming, are incompatible but complementary views of nature.     

Stiffening the stingray skeleton - an investigation of durophagy in myliobatid stingrays (Chondrichthyes, batoidea, myliobatidae)

The stingray family Myliobatidae contains five durophagous (hard prey specialist) genera and two planktivorous genera. A suite of morphological features makes it possible for the hard prey specialists to crush mollusks and crustaceans in their cartilaginous jaws. These include: 1) flat, pavement-like tooth plates set in an elastic dental ligament; 2) multiple layers of calcified cartilage on the surface of the jaws; 3) calcified struts running through the jaws; and 4) a lever system that amplifies the force of the jaw adductors. Examination of a range of taxa reveals that the presence of multiple layers of calcified cartilage, previously described from just a few species, is a plesiomorphy of Chondrichthyes. Calcified struts within the jaw, called "trabecular cartilage," are found only in the myliobatid genera, including the planktivorous Manta birostris. In the durophagous taxa, the struts are concentrated under the area where prey is crushed, thereby preventing local buckling of the jaws. Trabecular cartilage develops early in ontogeny, and does not appear to develop as a direct result of the stresses associated with feeding on hard prey. A "nutcracker" model of jaw function is proposed. In this model, the restricted gape, fused mandibular and palatoquadrate symphyses, and asynchronous contraction of the jaw adductors function to amplify the closing force by 2-4 times.     

Developmental pathways,homology and homonomy in metameric animals

Following Wagner's (1989) distinction between historical and biological concepts of homology, we analyze homology problems of metameric animals in the light of a biological concept. In identifying homology, we refer to the common informational background which two structures share. Therefore, homology relationships are matters of degree; they are ‘perfect’ only when there is full identity of informational background between the structures under comparison. Homonomy (serial homology) is not fundamentally different from other kinds of homology. We regard the differences between epimorphically and anamorphically developed segments as minor; therefore, the two kinds of segments are largely homologous. The morphogenetic processes giving rise to segmental structures are regarded as not necessarily hierarchical. We contrast the phylogenetic pattern of hierarchically nested homologies with a largely non-hierarchical pattern of homologous structures within the individual organism. This topological difference adds to heterochrony in generating the widespread mismatch of ontogeny and phylogeny.     

Meristem growth dynamics and branching patterns in the Cladoniaceae

Branching patterns in the lichen family Cladoniaceae are varied and taxonomically important. Branching occurs on the podetium, the erect secondary thallus that characterizes most species in the Cladoniaceae, and is influenced by growth dynamics of the fungal meristem tissue at the apex of the podetium. Branching is primarily the result of meristem divisions, and branching patterns are modified by meristem enlargement, deformation, and torsion. Branching processes are conserved, and early branch ontogeny provides information from which to determine relationships in the Cladoniaceae. Branching is characterized by two major patterns. In one pattern, branches arise from the relatively late divisions of a large meristem (≥100 μm in diameter), whose shape changes during ontogeny. In a second pattern, branches arise from small meristems (<100 μm in diameter), which split early in ontogeny but whose shape does not change. The trend toward reduced meristems that split early in ontogeny is seen as an evolutionary advance in the Cladoniaceae. Some "small meristem" species retain aspects of the "large meristem" habit in early ontogeny, and this provides a clue to their relationships. Patterns of meristem growth dynamics provide a basis for interpreting phylogeny in mycobionts of the Cladoniaceae. Meristem activities in four genera of the Cladoniaceae were compared in order to determine trends in growth dynamics within the family.     

Differences between inter- and intraspecific architectonic adaptations to pharyngeal mollusc crushing in cichlid fishes

Because fish heads are densely packed with muscles, ligaments, skeletal elements and other structures, transformations in one structure may influence surrounding structures. Transformations occur during phylogeny, ontogeny and as environmentally induced alterations, i.e. phenotypic plasticity. We describe differences in intra- and interspecific transformations of the pharyngeal jaw apparatus of haplochromine cichlids. Using multivariate clustering techniques we trace possible correlations in transformations of anatomical characters of the pharyngeal jaws and surrounding structures. The intraspecific transformation analysis is based on two environmentally induced morphs of Astatoreochromis alluaudi : a molluscivorous morph with a hypertrophied pharyngeal jaw apparatus and an insectivorous one with a non-hypertrophied apparatus. For the interspecific analysis five other haplochromine species from Lake Victoria with diets ranging from insects to molluscs were investigated. Although ranges in diet are the same, the anatomical ranges differ between A. alluaudi and the species cline. Besides similarities in anatomical changes of the pharyngeal jaw apparatus in the intra- and interspecific cline, differences were also observed. Apparently there are among haplochromines multiple pathways to achieve similar performance. In A. alluaudi architectonic and intrinsic plasticity constraints limit the adaptability of the pharyngeal jaw apparatus. In the species cline, these constraints have been overcome by genetical adaptation.     

Trait-dependency of trophic interactions in zooplankton food webs

Anthropogenic change in the abundance or identity of dominant top predators may induce reorganizations in whole food webs. Predicting these reorganizations requires identifying the biological rules that govern trophic niches. However, we still lack a detailed understanding of the respective contributions of body size, behaviour (e.g. match between predator hunting mode and prey antipredator strategy), phylogeny and/or ontogeny in determining both the presence and strength of trophic interactions. Here, we address this question by measuring zooplankton numerical response to fish predators in lake enclosures. We compared the fit to zooplankton count data of models grouping zooplankters based either on 1) body sizes, 2) antipredator behaviour, 3) body size combined with antipredator behaviour or on 4) phylogeny combined with ontogeny (i.e. different life stages of copepods). Body size was a better predictor of zooplankton numerical response to fish than antipredator behaviour, but combining body size and behaviour provided even better predictions. Models based on phylogeny combined with ontogeny clearly outperformed those based on other zooplankton grouping rules, except when phylogeny was poorly resolved. Removing ontogenetic information plagued the predictive power of the highly-resolved (genus-level) phylogenetic grouping but not of medium-resolved or poorly-resolved phylogenetic grouping. Our results support the recent use of phylogeny as a superior surrogate for traits controlling trophic niches, and further highlight the added value of combining phylogeny with ontogenetic traits. Further improvements in our mechanistic understanding of how trophic networks are shaped are bound to uncovering the trophic traits captured by phylogeny and ontogeny, but that currently remain hidden to us.     

Ballistic Beloniformes attacking through Snell's Window

Needlefishes (Beloniformes) were observed employing a range of stalking and attacking behaviours to attack schools of bait fishes ranging from the use of tactics common to predatory fishes to a novel behaviour: the use of leaping, aerial attacks. These aerial attacks are suggested to serve two purposes: to extend the attack range of the needlefishes and to reduce their prey's potential for evasion. Furthermore, a third purpose is hypothesized that the needlefishes are taking advantage of Snell's Window, an optical effect which may mask their approach to their prey.     

The development of the trigeminal jaw adductor musculature and associated skull elements in the lizard Podarcis sicula

The ontogenetic development of the jaw adductor musculature in Podarcis sicula (Raftnesque) is described in detail and related to patterns of ossification in associated skull elements. It was found that the coronoid bone ossifies in continuity with the developing bodenaponeurosis, whereas the elements of the upper temporal arcade ossify prior to (and seemingly independently of) the realization of an attachment of the developing jaw adductors.
Various aspects of the development of the jaw adductors are discussed in the light of theoretical claims concerning conflicting models of ontogeny, as is the role of ontogenetic studies in the determination of character polarity. It is concluded that the present study supports the model of epigenetic development, and that ontogeny alone is insufficient for the assessment of character polarity. Instead, ontogeny must be interpreted in the context of phylogenetic hypotheses.     

Ontogeny tends to recapitulate phylogeny in digital organisms

Abstract Biologists have long debated whether ontogeny recapitulates phylogeny and, if so, why. Two plausible explanations are that (i) changes to early developmental stages are selected against because they tend to disrupt later development and (ii) simpler structures often precede more complex ones in both ontogeny and phylogeny if the former serve as building blocks for the latter. It is difficult to test these hypotheses experimentally in natural systems, so we used a computational system that exhibits evolutionary dynamics. We observed that ontogeny does indeed recapitulate phylogeny; traits that arose earlier in a lineage's history also tended to be expressed earlier in the development of individuals. The relative complexity of traits contributed substantially to this correlation, but a significant tendency toward recapitulation remained even after accounting for trait complexity. This additional effect provides evidence that selection against developmental disruption also contributed to the conservation of early stages in development.     

Significance of epidermal fusion and intercalary growth for angiosperm evolution

The ancestral angiosperm flower probably had many separate elements in each floral whorl (sepals, petals, stamens and carpels). Derived character states include "fusion" of elements within a whorl (cohesion) and fusion between whorls (adhesion), as well as epigyny and the emergence of the other floral elements from the apex of the fused carpels. This article considers the roles of epidermal fusion and intercalary growth in the phylogeny and ontogeny of fused floral elements, and the importance of fusion for angiosperm evolution.     

Molecular systematics, biogeography and population structure of neotropical freshwater needlefishes of the genus Potamorrhaphis

Phylogenetic relationships of populations and species within Potamorrhaphis, a genus of freshwater South American needlefishes, were assessed using mitochondrial cytochrome b sequences. Samples were obtained from eight widely distributed localities in the Amazon and Orinoco rivers, and represented all three currently recognized species of Potamorrhaphis. The phylogeny of haplotypes corresponded imperfectly to current morphological species identities: haplotypes from P. guianensis, the most widespread species, did not make up a monophyletic clade. Geography played a strong role in structuring genetic variation: no haplotypes were shared between any localities, indicating restricted gene flow. Possible causes of this pattern include limited dispersal and the effects of current and past geographical barriers. The haplotype phylogeny also showed a complex relationship between fishes from different river basins. Based on the geographical distribution of clades, we hypothesize a connection between the middle Orinoco and Amazon via rivers of the Guianas. More ancient divergence events may have resulted from Miocene alterations of river drainage patterns. We also present limited data for two other Neotropical freshwater needlefish genera: Belonion and Pseudotylosurus. Pseudotylosurus showed evidence of substantial gene flow between distant localities, indicating ecological differences from Potamorrhaphis.     

Jaw morphology and ontogeny in five species of Ophryotrocha

Detailed scanning electron microscopy of jaws within the genus Ophryotrocha (Dorvilleidae, Annelida) was performed on 871 jaw parts. The investigations resulted in new understandings of the ontogeny and jaw morphology and have systematic implications for the family. Five species in the genus (Ophryotrocha alborana, O. diadema, O. gracilis, O. hartmanni, and O. labronica pacifica) were kept in culture, and the development of the jaws was studied by sampling throughout their life history. Ophryotrocha species have mandibular plates that remain the same throughout ontogeny, whereas the posterior shafts elongate. Both mandibular plate morphology and shaft ontogeny have species‐specific distinctions. In Ophryotrocha, the maxillae can be assigned to three to four distinct types, which are replaced by moulting. The maxillary morphology and developmental stages at which moults occur are species specific, although with broad intervals. A redefinition is given for some of the basic jaw elements, and new homologies are proposed for structures that are also present across other dorvilleid taxa. J. Morphol. 2010. © 2009 Wiley‐Liss, Inc.     

Les relations ontogenèse-phylogenèse:Applications paléontologiques

After a short historical introduction, the principal notions used to study the connections between ontogeny and phylogeny are desribed. The three fondamental standards (shape, age, size) upon which are made ontogenetic comparisons are defined and discussed.The different ontogenetic heterochronies are described and illustrated with concrete paleontological examples. Successively are studied:u

1. -dwarfirsm and giantism which are particularcases;
2. -the 4 types of heterochrony which affect somatic development (neoteny and acceleration) or sexual maturation (hypermorphosis and progenesis);
3. -the innovations which are a fast appearence of a new character and their associations with the 4 elementary heterochronies.

The heterochronies are connected with phylogeny. This leads to the definition of two fondamental tendancies: paedomorphosis and peramorphosis; the terms proterogenesis and palingenesis are redefined. To conclude, this study is inserted in a more wider context that shows the importance of ontogenetic knowledge to understand numerous evolutif processes (tempos in evolution, demographic strategies, cladism).     

Does evolutionary innovation in pharyngeal jaws lead to rapid lineage diversification in labrid fishes?

Background  

Major modifications to the pharyngeal jaw apparatus are widely regarded as a recurring evolutionary key innovation that has enabled adaptive radiation in many species-rich clades of percomorph fishes. However one of the central predictions of this hypothesis, that the acquisition of a modified pharyngeal jaw apparatus will be positively correlated with explosive lineage diversification, has never been tested. We applied comparative methods to a new time-calibrated phylogeny of labrid fishes to test whether diversification rates shifted at two scales where major pharyngeal jaw innovations have evolved: across all of Labridae and within the subclade of parrotfishes.