Ontogeny discombobulates phylogeny: paedomorphosis and higher-level salamander relationships

Evolutionary developmental biology ("evo-devo") has revolutionized evolutionary biology but has had relatively little impact on systematics. We show that similar large-scale developmental changes in distantly related lineages can dramatically mislead phylogenetic analyses based on morphological data. Salamanders are important model systems in many fields of biology and are of special interest in that many species are paedomorphic and thus never complete metamorphosis. A recent study of higher-level salamander phylogeny placed most paedomorphic families in a single clade based on morphological data. Here, we use new molecular and morphological data to show that this result most likely was caused by the misleading effects of paedomorphosis. We also provide a well-supported estimate of higher-level salamander relationships based on combined molecular and morphological data. Many authors have suggested that paedomorphosis may be problematic in studies of salamander phylogeny, but this hypothesis has never been tested with a rigorous phylogenetic analysis. We find that the misleading effects of paedomorphosis on phylogenetic analysis go beyond the sharing of homoplastic larval traits by paedomorphic adults, and the problem therefore is not solved by simply excluding suspected paedomorphic characters. Instead, two additional factors are critically important in causing paedomorphic species to be phylogenetically "misplaced": (1) the absence of clade-specific synapomorphies that develop during metamorphosis in nonpaedomorphic taxa and allow their "correct" placement and (2) parallel adaptive changes associated with the aquatic habitat of the larval stage. Our results suggest that the effects of paedomorphosis on phylogenetic analyses may be complex, difficult to detect, and can lead to results that are both wrong and statistically well supported by parsimony and Bayesian analyses.     

Heterochrony in Tingidae (Insecta: Heteroptera): paedomorphosis and/or peramorphosis?

Tingidae (Heteroptera: Insecta) exhibit cephalic tubercles that present a very diverse shape in larvae but that are much simpler in adults. A phylogeny based on adult and last instar characters showed that these tubercles evolved independently from simple to complex states in two clades, and reversed from complex to simple in some taxa. These homoplasies are analysed in the light of ontogenetic sequences and interpreted as heterochronic events. The general trend of evolution of the cephalic tubercles in Tingidae is in mosaic, and could be generally peramorphic, with some isolated cases of paedomorphosis.  Journal compilation © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 71–80. No claim to original French government works.     

Paedomorphosis as an Evolutionary Driving Force: Insights from Deep-Sea Brittle Stars

Heterochronic development has been proposed to have played an important role in the evolution of echinoderms. In the class Ophiuroidea, paedomorphosis (retention of juvenile characters into adulthood) has been documented in the families Ophiuridae and Ophiolepididae but not been investigated on a broader taxonomic scale. Historical errors, confusing juvenile stages with paedomorphic species, show the difficulties in correctly identifying the effects of heterochrony on development and evolution. This study presents a detailed analysis of 40 species with morphologies showing various degrees of juvenile appearance in late ontogeny. They are compared to a range of early ontogenetic stages from paedomorphic and non-paedomorphic species. Both quantitative and qualitative measurements are taken and analysed. The results suggest that strongly paedomorphic species are usually larger than other species at comparable developmental stage. The findings support recent notions of polyphyletic origin of the families Ophiuridae and Ophiolepididae. The importance of paedomorphosis and its correct recognition for the practice of taxonomy and phylogeny are emphasized.     

Paedomorphosis and heterochrony in the origin and evolution of the class holothuroidea

The role of paedomorphosis as a particular case of heterochrony in the origin and evolution of the class Holothuroidea is analyzed. It is shown that holothurians are characterized by the presence of some paedomorphic characters (reduced skeleton, absence of an axial complex in the shape of a morphologically integrated structure, single gonad with one gonopore). In many members of the subclass Holothuriacea, sclerites of the body wall are arranged in two layers. Sclerites of the deeper layer develop as a perforated plate and correspond to the skeletal elements forming in other echinoderms the body skeleton, for example, the test of sea urchins. Sclerites of the superficial layer frequently look like various tables, develop like spines of other echinoderm classes, in particular, juvenile tetraradiate spines of sea urchins, and correspond to spines of other classes of Echinodermata. Ontogenetic changes at the stage of five first tentacles resulted in interruption at an early stage of the development with the catastrophic metamorphosis, which is typical for other Eleutherozoa. The ontogeny of holothurians acquired the evolutive (gradual) character; the adult body began to develop on the basis of the larval body and larval tissues were partially included in the body of adult holothurians. As a result, the place and developmental pattern of the radial complex of organs changed and heterochrony in the development of characters concerned with different coordination chains intensified; therefore, the modern body plan of holothurians was formed. The processes of paedomorphosis and heterochrony played an important role not only in the origin and formation of the class Holothuroidea, but also during its evolution. Paedomorphic processes became rather important in the evolution of the order Synaptida. Paedomorphic features are particularly prominent in the structure of small interstitial forms. In some holothurians, the paedomorphosis resulted in the change in relationships between symmetry planes. The bilateral plane of symmetry of these holothurians coincide with the plane of symmetry 2–1–2, which is positioned in the majority of holothurians at about 72° to the bilateral plane. Independently, but frequently in parallel, the intestinal loop disappeared, so that the gut became straight and suspended on mediodorsal mesentery almost throughout its extent. The combination of these processes in holothurians of the order Synaptida resulted in the formation of almost complete pentaradially bilateral symmetry.     

A Relict Rhinesuchid (Amphibia: Temnospondyli) From The Lower Triassic Of South Africa

' Lydekkerina ' putterilli Broom from the Lystrosaurus Assemblage Zone (Middle Beaufort Group, South Africa) is shown to be a paedomorphic rhinesuchid ( Broomistega putterilli gen. nov.) rather than a lydekkerinid or juvenile stage of the rhinesuchid Uranocentrodon , as previously presumed. The most conspicuous characters, not related to its paedomorphic condition, include the shape of the parietals and the structure of the parasphenoid body and exoccipitals. The pattern of cranial growth changes in Broomistega has been investigated by comparison of the holotype with two hitherto undescribed immature specimens. For several characters referring to the size and position of the orbits, and re-modelling of the jugal proportions, retarded timing of growth transformations, compared to ontogenetic patterns in Permian rhinesuchids (typified by Muchocephalus ) is demonstrated. Some features of the evolution of the basicranial region of the skull, in the transition from rhinesuchids to more advanced capitosauroids, are re-evaluated. key words : temnospondyls, rhinesuchids, relict, paedomorphosis, growth changes.     

A New Extinct Genus of Cavioidea (Rodentia,Hystricognathi) from the Miocene of Patagonia (Argentina) and the Evolution of Cavioid Mandibular Morphology

The family Caviidae is represented in modern faunas by cavies and maras, whereas the family Hydrochoeridae is represented by capybaras. The evolutionary origin of these families has been related to a diversity of plesiomorphic fossil forms (recorded from the late Oligocene up to the middle Miocene) traditionally grouped in the family “Eocardiidae”. These fossil forms were included, together with Caviidae and Hydrochoeridae, within the Cavioidea s.s. (sensu stricto), because they share high crowned cheek teeth, double-hearted occlusal surface, short lower incisors, and moderate hystricognathy. Within Cavioidea s.s., caviids and hydrochoerids were interpreted as forming its crown group, because they have unique craniomandibular and dental features. In this contribution, a new taxon of Cavioidea s.s. from the middle Miocene of central Patagonia, Argentina, is described, and its phylogenetic position is determined on the basis of a morphological cladistic analysis in which “eocardiids” were included. The study permits the understanding of the sequence of appearance of characters that originated the highly divergent morphology of crown-group cavioids. The analysis of the sequence of appearance of the characters that traditionally diagnosed the crown group indicates that these changes did not occur at the same time. On the contrary, many of these features seem to have appeared at different nodes of the evolutionary history of Cavioidea s.s. The remarkably derived morphology of modern cavioids is the result of a stepwise appearance of a mosaic of evolutionary innovations that originated gradually along the history of Cavioidea during the late-middle Miocene.     

Evolution of morphological and behavioral ontogenies in females of a highly dimorphic clade of blennioid fishes

Comparison of ontogenetic trajectories with those inferred for ancestors provides a powerful but underused tool for the study of the evolution of different types of phenotypic characters. This approach was used to study morphological and behavioral evolution of the highly dimorphic chaenopsid genus Coralliozetus (Teleostei: Blennioidei). All sexually dimorphic synapomorphies of Coralliozetus involved evolution in females only; one character evolved via terminal addition (peramorphosis), whereas six evolved via terminal deletion (paedomorphosis). Evolution of the ontogeny of two behavioral characters (microhabitat use and feeding rate), as inferred by focal animal observations of eight species of tube blennies, was also confined to females and conformed to terminal deletion. Both sexes of outgroups and males of all species of Coralliozetus exhibit an ontogenetic shift from the open as juveniles to shelters as adults. However, females of all species of Coralliozetus retain the juvenile behavior of residing in the open. Blennies residing in the open take significantly more feeding bites than conspecifics residing in shelters, consequently, female Coralliozetus retain the high feeding rate of juveniles. Several of the paedomorphic morphological features of Coralliozetus females are plausibly associated with their paedomorphosis in microhabitat use. These include their reduced conspicuousness and reduced robustness compared to conspecific males. In groups such as chaenopsids, which undergo significant ontogenetic changes in microhabitat, paedomorphosis provides a mechanism for rapid coevolution of behavior and morphology. This study, the first to document the evolution of sexual dimorphism via both behavioral and morphological paedomorphosis, demonstrates the unique insights to be gained from a multidimensional analysis of phenotypic evolution.     

Evolution of salamander life cycles: a major-effect quantitative trait locus contributes to discrete and continuous variation for metamorphic timing

The evolution of alternate modes of development may occur through genetic changes in metamorphic timing. This hypothesis was examined by crossing salamanders that express alternate developmental modes: metamorphosis vs. paedomorphosis. Three strains were used in the crossing design: Ambystoma tigrinum tigrinum (Att; metamorph), wild-caught A. mexicanum (Am; paedomorph), and laboratory Am (paedomorph). Att/Am hybrids were created for each Am strain and then backcrossed to their respective Am line. Previous studies have shown that a dominant allele from Att (met(Att)) and a recessive allele from lab Am (met(lab)) results in metamorphosis in Att/Am hybrids, and met(Att)/met(lab) and met(lab)/met(lab) backcross genotypes are strongly associated with metamorphosis and paedomorphosis, respectively. We typed a molecular marker (contig325) linked to met and found that met(Att)/met(lab) and met(Att)/met(wild) were associated with metamorphosis in 99% of the cases examined. However, the frequency of paedomorphosis was 4.5 times higher for met(lab)/met(lab) than for met(wild)/met(wild). We also found that met(Att)/met(wild) and met(wild)/met(wild) genotypes discriminated distributions of early and late metamorphosing individuals. Two forms of phenotypic variation are contributed by met: continuous variation of metamorphic age and expression of discrete, alternate morphs. We suggest that the evolution of paedomorphosis is associated with genetic changes that delay metamorphic timing in biphasic life cycles.     

Ontogeny and phytogeny of the mesopodial skeleton in mosasauroid reptiles

Current phylogenics of mosasauroid reptiles are reviewed and a new phylogeny examining aigialosaur interrelationships presented. Patterns of mesopodial ossification and overall limb morphology are described for adult mosasauroids. Ossification sequences are mapped onto a phylogeny in order to assess the distribution of ontogenetic characters. Consistent and ordered distributions are found. Based on the phylogenetic distribution of ossification patterns, an overall mesopodial ossification sequence for mosasaurs is proposed. Carpal sequence: ulnare—distal carpal four (dc4)—intermedium—dc3—radiale or dc2—de1 or pisiform and dc5. Tarsal sequence: astragalus—distal tarsal four or calcaneum. Skeletal paedomorphosis is recognized as a dominant pattern in the evolution of mosasauroid limbs. Apomorphic characters of skeletal paedomorphosis, apparent in most taxa, reach extremes in tylosaurs. Arguments for the presence of a single proximal cartilage in the tarsus of mosasaurs are made. This cartilage is presumed to include ossification centres from which both the astragalus and calcaneum will ossify.     

Combinatorial model for the formation of body plans in higher metazoan taxa: Paleontological insight

The body plans of higher metazoan taxa were formed during a short time (on the geological time scale) by combination of the previously developed characters. The combinations were realized as a result of manifestation of latent characters in adults through various heterochronies. This resulted in mosaic evolution and concealment of intermediate forms. Many characters of new body plans appeared in the ancestral taxon and their various combinations in the newly established taxa formed the archaic diversity. The maximum rank of newly appearing higher taxa decreased with geological time. The evolution of metazoans passed from the development of the general body plan to less significant details and appearance of body plans describing taxa of lower ranks. New body plans of higher taxa were superposed on the old body plan rather than replaced it, extending with time the subordination of body plans and respective hierarchy of taxa. Aromorphoses are always connected with the appearance of a new body plan. The appearance of new taxa and an increase in morphological diversity mostly occurred at certain boundaries in the development of the biota, which were connected with a sharp increase in the previously limited resources.     

Facultative paedomorphosis and the pattern of intra- and interspecific variation in cranial skeleton: lessons from European newts (Ichthyosaura alpestris and Lissotriton vulgaris)

Paedomorphosis, the presence of ancestral larval and juvenile traits that occur at the descendent adult stage, is an evolutionary phenomenon that shaped morphological evolution in many vertebrate lineages, including tailed amphibians. Among salamandrid species, paedomorphic and metamorphic phenotypes can be observed within single populations (facultative paedomorphosis). Despite wide interest in facultative paedomorphosis and polymorphism produced by heterochronic changes (heterochronic polymorphism), the studies that investigate intraspecific morphological variation in facultative paedomorphic species are largely missing. By quantifying the cranium size and development (bone development and remodeling), we investigated the variation at multiple levels (i.e., between sexes, populations and species) of two facultatively paedomorphic European newt species: the alpine and the smooth newt. The pattern of variation between paedomorphs (individuals keeping larval traits at the adult stage) and metamorphs (metamorphosed adult individuals) varied between species and among populations within a single species. The patterns of variation in size and skull formation appear to be more uniform in the alpine than in the smooth newt, indicating that developmental constraints differed between species (more pronounced in alpine than in smooth newt). Our study shows that the cranial skeleton provides detailed insight in the pattern of variation and divergence in heterochronic polymorphism within and between species and open new questions related to heterochronic polymorphism and evolution of cranial skeleton.     

HETEROCHRONY AND HETEROBLASTIC LEAF DEVELOPMENT IN TWO SUBSPECIES OF CUCURBITA ARGYROSPERMA (CUCURBITACEAE)

To date, reports of paedomorphosis at the whole plant or shoot level have been loosely based on whole plant form or on the sequence of leaf shapes produced along the shoot (heteroblasty). However, interpreting the significance of heterochrony in the evolutionary loss or gain of heteroblasty based on mature leaf forms assumes that all leaves with the same shape arose through very similar modes of organogenesis. This study examines this assumption in two subspecies of Cucurbita argyrosperma, one that is wild and heteroblastic and a second that is cultivated and not markedly heteroblastic. All leaves of the cultivar are visually similar to early leaves of the wild subspecies. The cultivar is considered to be the progenitor of the wild subspecies. Scanning electron microscopy and allometry of developing leaves showed that at early nodal positions along the primary shoot, leaf development in both subspecies was similar. At later nodal positions, very young leaves of both subspecies were more similar to each other than to leaves at earlier nodal positions within the same plant at the same stage of development. This early similarity was masked in the mature shapes of later leaves due to subsequent differences in allometric growth. Thus a simple hypothesis of paedomorphosis in which the early leaf form in the progenitor is simply reiterated at later nodal positions in the cultivar is not supported by patterns of leaf development.     

Morphogenesis Rate Variability and Modularity of Development in Jurassic Ammonites of the Genus Arcticoceras Spath, 1924

The high variability of ammonites is largely due to the diversity of combinations of individual heterochronies (bradimorphy, tachymorphy, bradygeronty, and tachygeronty) and the modularity of development. Using the genus Arcticoceras as an example, it was shown that heterochronies of various directions can be combined in any number of characters, and individual heterochronies differ from phylogenetic ones by their smaller range, and a larger number of combinations. The study of such combinations allowed intraspecific morphs to be recognized, and available Arcticoceras species to be revised. During the Early and Middle Bathonian, the family Cardioceratidae evolved through a series of paedomorphosis, and after the appearance of Cadoceratinae, through accelerations.     

Huehuecuetzpalli mixtecus gen. et sp. nov: a basal squamate (Reptilia) from the Early Cretaceous of Tepexi de Rodríguez,Central México

Huehuecuetzpalli mixtecus gen. et sp. nov. is characterized by a combination of characters unlike those of any of the previously described Late Jurassic or Early Cretaceous lizards. It has most of the synapomorphies common to modern squamates, but still retains primitive features rare in living taxa. Autapomorphic characters include an anteroposteriorly elongated premaxilla that results in the elongation of the snout and the apparent retraction of the external nares. A small rounded postfrontal and a parietal foramen on the frontoparietal suture suggest affinities with iguanians, but the retention of divided premaxillae, amphicoelous vertebrae, thoracolumbar intercentra, entepicondylar foramen, and a second distal tarsal supports the hypothesis that Huehuecuetzpalli has a more basal position relative to the extant squamates. Although its appearance is late in the fossil record of lizards, Huehuecuetzpalli is the first report of a basal squamate. It provides important information on early transformation of characters in lizard evolution. Many primitive characters present in some modern squamates are usually explained by paedomorphosis; however, these characters are common in early lizards suggesting that derived states may have been fixed later in lizard evolution. If Huehuecuetzpalli is an iguanian, then it would be the earliest known representative of this lineage and extends their fossil record into the Albian. This paper presents an extensive review of the characters and character states used in previously published cladistic analyses of the Squamata.     

Stabilizing and directional selection on facial paedomorphosis

Averageness is purportedly the result of stabilizing selection maintaining the population mean, whereas facial paedomorphosis is a product of directional selection driving the population mean towards an increasingly juvenile appearance. If selection is predominantly stabilizing, intermediate phenotypes reflect high genetic quality and mathematically average faces should be found attractive. If, on the other hand, directional selection is strong enough, extreme phenotypes reflect high genetic quality and juvenilized faces will be found attractive. To compare the effects of stabilizing and directional selection on facial paedomorphosis (juvenilization), graphic morphing and editing techniques were used to alter the appearance of composite faces to make them appear more or less juvenile. Both facial models and judges of attractiveness were from the CSU-Long Beach campus. Although effect sizes for both preferences were large, the effect for averageness was nearly twice that found for juvenilization, an indication that stabilizing selection influences preferences for facial paedomorphosis more so than directional selection in contemporary humans.     

Seasonal variation of morph ratio in facultatively paedomorphic populations of the palmate newt Triturus helveticus

Facultative paedomorphosis is a polyphenism in which individuals may express one of two alternative ontogenetic pathways (metamorphosis vs. paedomorphosis) depending on environmental cues. Previous laboratory experiments showed that drying can cause morph ratio change, suggesting that the maintenance of facultative paedomorphosis is highly dependent on environmental determinants. The aim of this study was to examine seasonal variation in morph ratios in eight ponds from Larzac (southern France) naturally inhabited by palmate newts and to relate it to pond drying. In some ponds, the relative proportion of paedomorphs (i.e. individuals retaining gills at the adult stage) increased after the breeding period, but it remained stable or decreased in other ponds. This seasonal variation in the abundance of the two morphs most probably reflects (1) the emigration of metamorphs leaving the pond to occupy terrestrial habitats and (2) metamorphosis of paedomorphic adults in response to drying of the ponds. This study shows that facultative paedomorphosis in palmate newts is a dynamic process that allows rapid change (i.e. within a single year) in morph ratio to fit environmental variation (i.e. risk of drying) within the aquatic habitats. Long-term studies are needed to model the evolution of the dimorphism according to environmental change.     

Saltatory Processes and Altricial to Precocial Forms in the Ontogeny of Fishes

SYNOPSIS. Development is not a gradual but a saltatory process.A combination of qualitative changes in form and function—thresholds—createsboundaries between a succession of quantitative intervals—steps.Thresholds can be modified by an altered time of appearanceof structures and functions (heterochrony), especially duringearly ontogeny, to form an operational basis for the prolongationof juvenile characters and adaptability into later ontogeny.Whereas such prolongation enables juvenilization in phylogeny,analogous principles may operate on a much shorter time scaleto produce the r-selection-like altricial and the K-selection-likeprecocial trends in ontogeny. The inherited capacity to adjustconstantly to the environment (heterochrony) selects for structural,biochemical and behavioral improvements. The tendency is towardthe precocial but the way back to altricial forms is left open.The heterochronous adaptations in early ontogeny can "reverse"the vulnerable specialization, should the environment becomeless stable and/or the community less competitive. Juvenilization,capable of turning gerontomorphosis into paedomorphosis in evolution,and heterochronous shifts of character anlagen, capable of turninga precocial trend into an altricial trend in ontogeny are bothpart of the same biological process which operates during earlyontogeny.     

早期形态发生:一种解决贻贝科(软体动物门:双壳纲)分类、系统发育和进化问题的方法

作者对贻贝科贝类的幼虫和幼贝期发育阶段形态结构的出现和变化顺序进行了研究,其约60个不同分类单元的个体发生可归纳为4种形态发生类型或模式。主要对3个形态发生区域的阶段形态结构的起源、发育变化和同源性做了研究。其一,即中央区域,开始形成于前双壳Ⅰ期(PD-Ⅰ),在某个分类单元它可以在前双壳Ⅱ期(PD-Ⅱ)和幼贝期(N)形成,而在其它分类单元则在前双壳Ⅱ期、幼贝期和双壳期(D)形成;第二区域,即背部后区,在幼贝期出现;第三区域,即背部前区,出现于双壳期。双壳期背部后区在某个分类单元起源于幼贝期的形态构造,在其它分类单元则可能起源于双壳期的形态构造。与在贻贝分类学上应用的成体特征相比,早期发育阶段中央和背部后区的形态结构显示出很明显的发育顺序或特征变化规律。根据以前人们熟知而尚未应用到分类和系统发育研究中的早期发育阶段形态特征,作者重新修订了Soot-Ryen的现生贻贝科种上阶元分类系统,重新提出了科内系统发育关系。修订的分类系统表明,Scarlato and Starobogatov(1984)提出的贻贝科各亚科由偏顶蛤亚科开始,沿4条系统发育路线演化发展,对应其早期发育阶段的4类形态发生类型或模式。     

Chordate Evolution and Autonomous Specification of Cell Fate: The Ascidian Embryo Model

SYNOPSIS. Two parallel themes emerge in the history of the investigationof the ascidian tunicate [Urochordata] embryo: the realizationthat the larval stage is probably a surviving example of theearliest chordate body plan from which vertebrates arose, andsecondly the unusual degree of autonomous specification of cellfate involved in the development of ascidian larval parts. Suchdevelopmental autonomy in larval structures results in patternsof development referred to as "mosaic." This paper follows theprogress of these two themes from their beginnings in the secondhalf of the nineteenth century to their status at the presenttime. Romer's concept of vertebrates as a "dual animal" (somaticand visceral) stands out as a landmark perception in supportof the theory of vertebrate origin by paedomorphosis througha merger of the pelagic larval and benthic adult stages of atunicate-like animal. The present contribution attempts to unitethe two themes by postulating that autonomous specificationfurther enhanced the modular nature of the developing tunicateembryo and permitted natural selection to act differentiallyon the largely independent organ systems of larvae and paedomorphs,in what amounts to a mosaic selection pattern. This, in turn,favored the very rapid emergence and radiation of the chordatesduring the Cambrian explosion.