Short- and long-term consequences of thermal variation in the larval environment of anurans

1. To survive adverse or unpredictable conditions in the ontogenetic environment, many organisms retain a level of phenotypic plasticity that allows them to meet the challenges of rapidly changing conditions. Larval anurans are widely known for their ability to modify behaviour, morphology and physiological processes during development, making them an ideal model system for studies of environmental effects on phenotypic traits. Although temperature is one of the most important factors influencing the growth, development and metamorphic condition of larval anurans, many studies have failed to include ecologically relevant thermal fluctuations among their treatments. 2. We compared the growth and age at metamorphosis of striped marsh frogs Limnodynastes peronii raised in a diurnally fluctuating thermal regime and a stable regime of the same mean temperature. We then assessed the long-term effects of the larval environment on the morphology and performance of post-metamorphic frogs. 3. Larval L. peronii from the fluctuating treatment were significantly longer throughout development and metamorphosed about 5 days earlier. Frogs from the fluctuating group metamorphosed at a smaller mass and in poorer condition compared with the stable group, and had proportionally shorter legs. 4. Frogs from the fluctuating group showed greater jumping performance at metamorphosis and less degradation in performance during a 10-week dormancy. Treatment differences in performance could not be explained by whole-animal morphological variation, suggesting improved contractile properties of the muscles in the fluctuating group.     

Ontogeny, phylogeny, and morphology in anuran larvae: morphometric analysis of cranial development and evolution in Rana tadpoles (Anura: Ranidae)

Comparative studies of chondrocranial morphology in larval anurans are typically qualitative in nature, focusing primarily on discrete variation or gross differences in the size or shape of individual structures. Detailed data on chondrocranial allometry are currently limited to only two species, Rana sylvatica and Bufo americanus. This study uses geometric morphometric and multivariate statistical analyses to examine interspecific variation in both larval chondrocranial shape and patterns of ontogenetic allometry among six species of Rana. Variation is interpreted within the context of hypothesized phylogenetic relationships among these species. Canonical variates analyses of geometric morphometric datasets indicate that species can be clearly discriminated based on chondrocranial shape, even when whole ontogenies are included in the analysis. Ordinations and cluster analyses based on chondrocranial shape data indicate the presence of three primary groupings (R. sylvatica; R. catesbeiana + R. clamitans; and R. palustris + R. pipiens + R. sphenocephala), and patterns of similarity closely reflect phylogenetic relationships. Analysis of chondrocranial allometry reveals that some patterns are conserved across all species (e.g., most measurements scale with negative allometry, those associated with the posterior palatoquadrate tend to scale with isometry or positive allometry). Ontogenetic scaling along similar allometric trajectories, lateral transpositions of individual trajectories, and variable allometric relationships all contribute to shape differences among species. Overall patterns of similarity among ontogenetic trajectories also strongly reflect phylogenetic relationships. Thus, this study demonstrates a tight link between ontogeny, phylogeny, and morphology, and highlights the importance of including both ontogenetic and phylogenetic data in studies of chondrocranial evolution in larval anurans.     

Precopulatory behaviour and the evolutionary relationships of Discoglossidae

The phylogenetic relationships among primitive anurans remain controversial, even when several morphological and molecular approaches have been used in an attempt to resolve them. Nevertheless, very little effort has been made to study these relationships with behavioural data. We studied the relation between some precopulatory behaviour characters (male call characteristics and call recognition by females) and the different proposed phylogenies among the anuran genera Alytes, Discoglossus and Bombina . Different acoustic variables were analysed from male calls of different species of these genera; Alytes cisternasii females were used in recognition tests with calls from those species. A phenetic tree generated from male call characteristics grouped Bombina with Discoglossu s and separated these two genera from Alytes, although the tree generated from female response data did not show such a clear result. A. cisternasii females are mostly using some features that are absent in Alytes calls in order to recognize male calls. The two characters, mapped onto the three alternative phylogenetic proposals, did not resolve the trichotomy among the three genera, but suggested that the studied behavioural characters have a clear phylogenetic load.     

The amphibian octavo-lateralis system and its regressive and progressive evolution

The phylogenetic and ontogenetic changes in the octavolateralis system of sarcopterygian fish and tetrapods, presumed to be important for the formation of an amphibian auditory system, are reviewed. The lateral line system shows rudimentation of lines and loss of ampullary electroreceptors in many amphibians; in some amphibians it never develops. The metamorphic changes of the lateral-line system show different patterns in the different amphibian lineages with metamorphic retention in most urodeles and metamorphic loss in most anurans. The multitude of both ontogenetic and phylogenetic changes of the lateral line system among amphibians do exclude any prediction as to how this system might have changed in ancestral amniotes. The most important auditory epithelium of the tetrapod inner ear, the basilar papilla, seems to be primitively present in all tetrapods and Latimeria. In two amphibian lineages there is a trend towards rudimentation and loss of the basilar papilla. Only in the third order, the anurans, a tympanic ear develops and the inner ear shows a progressive evolution of the auditory epithelia. Together with the known differences in the periotic labyrinth of amphibians and amniotes, this scenario suggests a parallel evolution of the amniotic and anuran auditory periphery. All mechanoreceptive hair cells of the lateral line system and the inner ear appear to receive a common and bilateral efferent innervation. Among amphibians this pattern is represented only in some urodeles, whereas anurans show a derived pattern with loss of a bilateral component and presumably also of a common neuromast/inner ear component. Changes in the rhombencephalic nuclei which receive octavo-lateralis afferent fibers show a trend towards development of auditory nuclei only in the anuran lineage. The phylogenetic appearance of an auditory nucleus in this lineage coincides with the complete absence of formation of ampullary electroreceptors. In contrast, the earlier claim of a correlation between a metamorphic loss of the lateral line system and the formation of an auditory nucleus is not supported by more recent data: an auditory nucleus develops in anurans already prior to metamorphosis and is present in all anurans even when they retain the neuromast system. In anurans with a metamorphic loss of the neuromasts, the second order neurons degenerate as well. This independence of the auditory and the second order lateral line nuclei is further substantiated by their separate projection to other brain areas, like the torus semicircularis of the midbrain, and their functional properties.(ABSTRACT TRUNCATED AT 400 WORDS)     

我国蝌蚪的科级分类研究

2017年末,我国的两栖动物已记录3目14科466种,其中,无尾目Anura 10科386种。蝌蚪是无尾两栖类物种的幼体,具有一系列适应水生生活的形态特征和一个特别的变态过程,是无尾目的主要标志之一。我国蝌蚪的形态特征散见于各个物种的形态描述,而对蝌蚪科级分类的系统研究却阙如。本文基于蝌蚪的8个形态学分类性状,概述了我国除亚洲角蛙科Ceratobatrachidae外9个科(铃蟾科Bombinatoridae、角蟾科Megophryidae、蟾蜍科Bufonidae、雨蛙科Hylidae、蛙科Ranidae、叉舌蛙科Dicroglossidae、浮蛙科Occidozygidae、树蛙科Rhacophoridae、姬蛙科Microhylidae)的蝌蚪分类特征,系统阐述了蝌蚪科级分类特征的分类和适应意义。     

Ontogenetic phenotypic plasticity during the reproductive phase in Arabidopsis thaliana (Brassicaceae)

While phenotypic plasticity has been the focus of much research and debate in the recent ecological and evolutionary literature, the developmental nature of the phenomenon has been mostly overlooked. A developmental perspective must ultimately be an integral part of our understanding of how organisms cope with heterogeneous environments. In this paper I use the rapid cycling Arabidopsis thaliana to address the following questions concerning developmental plasticity. (1) Are there genetic and/or environmental differences in parameters describing ontogenetic trajectories? (2) Is ontogenetic variation produced by differences in genotypes and/or environments for two crucial traits of the reproductive phase of the life cycle, stem elongation and flower production? (3) Is there ontogenetic variability for the correlation between the two characters? I found genetic variation, plasticity, and variation for plasticity affecting at least some of the growth parameters, indicating potential for evolution via heterochronic shifts in ontogenetic trajectories. Within-population differences among families are determined before the onset of the reproductive phase, while among-population variation is the result of divergence during the reproductive phase of the ontogeny. Finally, the ontogenetic profiles of character correlations are very distinct between the ecologically meaningful categories of early- and late-flowering “ecotypes” in this species, and show susceptibility to environmental change.     

Patterns of carpal development among anuran amphibians

The unity and diversity of developmental processes in the vertebrate limb have singular importance in the interpretation of evolutionary hypotheses of tetrapod diversification. In anurans, the intraordinal diversity of forelimbs seems to be related to the fusion of distal carpals, whereas proximal carpals are invariable. However, there are different ontogenetic pathways involved in the differentiation of proximal carpals. This study presents a comparative analysis of early developmental features in one archeobatrachian and 23 neobatrachian species representing five families and explores the variability in the differentiation of carpal cartilages. We found new evidence supporting the presence of an embryonic intermedium that incorporates with the ulnare. Difference between the pipid Xenopus and the neobatrachians is interpreted as a change in the rate of differentiation of Distal Carpal 5 that does not affect the developmental pattern of digits. The developmental variability exhibited by the intermedium, radiale, and Element Y is combined in patterns that converge on the same adult carpal morphology among neobatrachians; these patterns appear to contain potentially useful phylogenetic information.     

MULTILEVEL ANALYSIS OF MORPHOMETRIC DATA FROM NATURAL PLANT POPULATIONS: INSIGHTS INTO ONTOGENETIC,GENETIC, AND SELECTIVE CORRELATIONS IN DALECHAMPIA SCANDENS

I examined patterns of covariation of three morphometric blossom characters [gland area (GA), gland–stigma distance (GSD), and bract length (BL)] within genets, among genets, and among populations of the tropical vine, Dalechampia scandens (Euphorbiaceae). Covariance between BL and GA was evenly distributed among the three levels. This observation, coupled with developmental information, indicates that the two characters change size similarly during development, that there is probably genetic covariance between them (apparently caused by pleiotropy), and that the genetic covariance may have constrained (at least proximally) the course of population differentiation with respect to these characters. Most covariance between GSD and GA occurred at the among-population level. This observation, coupled with developmental information, indicates that there is negligible ontogenetic covariance and that within populations there is probably little or no genetic covariance between the two characters. Among-population covariance has probably been caused by natural selection operating in a correlated fashion on characters that functionally interact in pollination.     

The impact of larval predators and competitors on the morphology and fitness of juvenile treefrogs

Studies of phenotypic plasticity typically focus on traits in single ontogenetic stages. However, plastic responses can be induced in multiple ontogenetic stages and traits induced early in ontogeny may have lasting effects. We examined how gray treefrog larvae altered their morphology in four different larval environments and whether different larval environments affected the survival, growth, development, and morphology of juvenile frogs at metamorphosis. We then reared these juveniles in terrestrial environments under high and low intraspecific competition to determine whether the initial differences in traits at metamorphosis affected subsequent survival and growth, whether the initial phenotypic differences converged over time, and whether competition in the terrestrial environment induced further phenotypic changes. Larval and juvenile environments both affected treefrog traits. Larval predators induced relatively deep tail fins and short bodies, but there was no impact on larval development. In contrast, larval competitors induced relatively short tails and long bodies, reduced larval growth, and slowed larval development. At metamorphosis, larval predators had no effect on juvenile growth or relative morphology while larval competitors produced juveniles that were smaller and possessed relatively shorter limbs and shorter bodies. After 1 month of terrestrial competition among the juvenile frogs, the initial differences in juvenile morphology did not converge. There were no differences in growth due to larval treatment but there were differences in survival. Individuals that experienced low competition as tadpoles experienced near perfect survival as juvenile frogs but individuals that experienced high competition as tadpoles suffered an 18% decrease in survival as juvenile frogs. There were also morphological responses to juvenile competition, but these changes appear to be due, at least in part, to allometric effects. Collectively, these results demonstrate that larval environments can have profound impacts on the traits and fitness of organisms later in ontogeny.     

Phylogenetic interpretation of ontogenetic change: sorting out the actual and artefactual in an empirical case study of centrarchid fishes

Hypothesized relationships between ontogenetic and phylogenetic change in morphological characters were empirically tested in centrarchid fishes by comparing observed patterns of character development with patterns of character evolution as inferred from a representative phylogenetic hypothesis. This phylogeny was based on 56–61 morphological characters that were polarized by outgroup comparison. Through these comparisons, evolutionary changes in character ontogeny were categorized in one of eight classes (terminal addition, terminal deletion, terminal substitution, non-terminal addition, non-terminal deletion, non-terminal substitution, ontogenetic reversal and substitution). The relative frequencies of each of these classes provided an empirical basis from which assumptions underlying hypothesized relationships between ontogeny and phylogeny were tested. In order to test hypothesized relationships between ontogeny and phylogeny that involve assumptions about the relative frequencies of terminal change (e.g. the use of ontogeny as a homology criterion), two additional phylogenies were generated in which terminal addition and terminal deletion were maximized and minimized for all characters. Character state change interpreted from these phylogenies thus represents the maxima and minima of the frequency range of terminal addition and terminal deletion for the 8.7 × 10³⁶ trees possible for centrarchids. It was found for these data that terminal change accounts for c. 75% of the character state change. This suggests either that early ontogeny is conserved in evolution or that interpretation and classification of evolutionary changes in ontogeny is biased in part by the way that characters are recognized, delimited and coded. It was found that ontogenetic interpretation is influenced by two levels of homology decision: an initial decision involving delimitation of the character (the ontogenetic sequence), and the subsequent recognition of homologous components of developmental sequences. Recognition of phylogenetic homology among individual components of developmental sequences is necessary for interpretation of evolutionary changes in ontogeny as either terminal or non-terminal. If development is the primary criterion applied in recognizing individual homologies among parts of ontogenetic sequences, the only possible interpretation of phylogenetic differences is that of terminal change. If homologies of the components cannot be ascertained, recognition of the homology of the developmental sequence as a whole will result in the interpretation of evolutionary differences as substitutions. Particularly when the objective of a study is to discover how ontogeny has evolved, criteria in addition to ontogeny must be used to recognize homology. Interpretation is also dependent upon delimitation within an ontogenetic sequence. This is in part a function of the way that an investigator ‘sees’ and codes characters. Binary and multistate characters influence interpretation differently and predictably. The use of ontogeny for determining phylogenetic polarity as previously proposed rests on the assumptions that ancestral ontogenies are conserved and that character evolution occurs predominantly through terminal addition. It was found for these data that terminal addition may comprise a maximum of 51.9% of the total character state change. It is concluded that the ontogenetic criterion is not a reliable indicator of phylogenetic polarity. Process and pattern data are collected simultaneously by those engaged in comparative morphological studies of development. The set of alternative explanatory processes is limited in the process of observing development. These form necessary starting points for the research of developmental biologists. Separating ‘empirical’ results from interpretational influences requires awareness of potential biases in the course of character selection, coding and interpretation. Consideration of the interpretational problems involved in identifying and classifying phylogenetic changes in ontogeny leads to a re-evaluation of the purpose, usefulness and information conveyed by the current classification system. It is recommended that alternative classification schemes be pursued.     

Allometric relations in three species of finches (Aves: Fringillidae)

Static nestling, adult and ontogenetic allometry were analysed in three species of finches. Static nestling allometry was very similar across age in early ontogeny and among species and could be approximated by a single matrix of phenotypic variances and covariances. The first eigenvector of this matrix showed negative allometry of bill and tarsus to mass, but positive for wing length to mass. Adult static allometry was also very similar among species, but differed from nestling pattern. In adults the bill had a positive allometry in relation to tarsus and wing, but negative to mass, while tarsus and wing were unrelated to mass. The ontogenetic allometry in each species was very similar to nestling static allometry. Viewed in relation to final size, bill characters grew more slowly than body characters, but for a longer time, which created the difference between adult and nestling allometric patterns. There were differences among species both with regard to elevation and slope of allometric coefficients, suggesting that the differences among species came about by changes in the three fundamental ontogenetic parameters namely growth rate, onset of growth and offset of growth.     

Individual ontogenetic trajectories and ontogenetic channels of three forms of large African barbs (<Emphasis Type="Italic">Barbus intermedius</Emphasis> complex). Analysis of experimental data

Changes of external morphological characters in three forms (morphotypes) of African barbs from Lake Tana (Ethiopia) belonging to Barbus intermedius complex were traced using electronic tags. It was shown that within age interval from two to four years individual ontogenetic allometric curves often cannot be described with a single power function equation. Individual ontogenetic trajectories in the principal components space within this interval strongly differ in shape meandering within ontogenetic channels outlined on the basis of cross-sectional data. Morphological differences between siblings are found that do not allow to classify some of them with the morphotype of their parents.     

Archaeobatrachian paraphyly and pangaean diversification of crown-group frogs

Current models for the early diversification of living frogs inferred from morphological, ontogenetic, or DNA sequence data invoke very different scenarios of character evolution and biogeography. To explore central controversies on the phylogeny of Anura, we analyzed nearly 4000 base pairs of mitochondrial and nuclear DNA for the major frog lineages. Likelihood-based analyses of this data set are congruent with morphological evidence in supporting a paraphyletic arrangement of archaeobatrachian frogs, with an (Ascaphus + Leiopelma) clade as the sister-group of all other living anurans. The stability of this outcome is reinforced by screening for phylogenetic bias resulting from site-specific rate variation, homoplasy, or the obligatory use of distantly related outgroups. Twenty-one alternative branching and rooting hypotheses were evaluated using a nonparametric multicomparison test and parametric bootstrapping. Relaxed molecular clock estimates situate the emergence of crown-group anurans in the Triassic, approximately 55 million years prior to their first appearance in the fossil record. The existence of at least four extant frog lineages on the supercontinent Pangaea before its breakup gains support from the estimation that three early splits between Laurasia- and Gondwana-associated families coincide with the initial rifting of these landmasses. This observation outlines the potential significance of this breakup event in the formation of separate Mesozoic faunal assemblages in both hemispheres.     

Developmental characters in phylogenetic inference and their absolute timing information

Despite the recent surge of interest in studying the evolution of development, surprisingly little work has been done to investigate the phylogenetic signal in developmental characters. Yet, both the potential usefulness of developmental characters in phylogenetic reconstruction and the validity of inferences on the evolution of developmental characters depend on the presence of such a phylogenetic signal and on the ability of our coding scheme to capture it. In a recent study, we showed, using simulations, that a new method (called the continuous analysis) using standardized time or ontogenetic sequence data and squared-change parsimony outperformed event pairing and event cracking in analyzing developmental data on a reference phylogeny. Using the same simulated data, we demonstrate that all these coding methods (event pairing and standardized time or ontogenetic sequence data) can be used to produce phylogenetically informative data. Despite some dependence between characters (the position of an event in an ontogenetic sequence is not independent of the position of other events in the same sequence), parsimony analysis of such characters converges on the correct phylogeny as the amount of data increases. In this context, the new coding method (developed for the continuous analysis) outperforms event pairing; it recovers a lower proportion of incorrect clades. This study thus validates the use of ontogenetic data in phylogenetic inference and presents a simple coding scheme that can extract a reliable phylogenetic signal from these data.     

A description of larval and early juvenile development in Paralomis spinosissima (Decapoda: Anomura: Paguroidea: Lithodidae) from South Georgia waters (Southern Ocean)

The early ontogenetic stages of Paralomis spinosissima Birstein and Vinogradow, 1972, are described in detail and illustrated, with notes on morphological variability observed. Larval and early juvenile development was described to the crab I instar reared under controlled conditions of temperature and food supply. The abbreviated larval development invariably passed through two zoeal stages and the benthic megalopa stage. The larval development was completed without food supply, and food Artemia nauplii were first given after moult to the crab-I stage. Simplification and retarded development of the mouthparts are discussed as a function of lecithotrophy of these larvae and based on morphology no facultative feeding mode is suggested. Lecithotrophy in the Southern Ocean Lithodidae is discussed to be an adaptation allowing independence from seasonal food availability at high latitudes.     

Morphological Variations within the Ontogeny of Deinonychus antirrhopus (Theropoda,Dromaeosauridae)

This research resulted from the determination that MCZ 8791 is a specimen of Deinonychus antirrhopus between one and two years of age and that the morphological variations within particular growth stages of this taxon have yet to be described. The primary goal of the research is to identify ontogenetic variations in this taxon. Histological analyses determined that the Deinonychus specimens AMNH 3015 and MOR 1178 were adults. Comparisons are made between MCZ 8791 and these adult specimens. The holotype, YPM 5205, and the other associated specimens of this taxon within the YPM collection are similar in size and morphology to AMNH 3015. Further comparisons were made with the three partial specimens OMNH 50268, MCZ 4371, and MOR 1182. Although these specimens represent only a partial ontogenetic series, a number of morphological variations can be described. One secondary goal of this research is to compare the known pattern of variable, informative, ontogenetic characters in MCZ 8791 to a similar pattern of morphological characters in the sub-adult dromaeosaurid specimen Bambiraptor feinbergorum, AMNH FR: 30556. If the characters that have been determined to represent variable juvenile morphology in the ontogeny of Deinonychus are exhibited in Bambiraptor, this study will begin the process of determining whether a similar, conservative, ontogenetic pattern exists throughout the rest of Dromaeosauridae. If defensible, it may reduce the number of sympatric taxa within this clade. The other secondary goal relates to the forelimb function. The approximate body size, forelimb length, wrist development, and the presence of a more prominent olecranon on the ulna of MCZ 8791 support the hypothesis that juveniles of this taxon possessed some form of flight capability.     

The evolution of anther morphology in orchids: incumbent anthers, superposed pollinia, and the vandoid complex

The anther is the source of several of the principal characters traditionally used for classification in Orchidaceae, especially in Epidendroideae. In particular, anther and pollinium orientation are important, but little-studied characters; it is not known whether various instances of these states are achieved in the same way. We examined variation in anther and pollinium orientation in Epidendroideae and Vanilloideae using anatomical sections of columns at successive ontogenetic stages and related the observed changes to the final anther morphology to reexamine our homology hypotheses for these characters. Anther bending in vanilloids is achieved primarily by massive expansion of the connective. In nonvandoid epidendroids it is the result of column elongation and tipping of the mature anther, while in vandoids it is due to a redirection of growth in very early ontogenetic stages. Superposed pollinia result from a reorientation of developing thecae; those is Sobralia result from incurving of the thecae, while vandoids have thecae that are directed outward (latrorse). Contrasting ontogenetic and phylogenetic patterns suggest heterochronic changes in these characters, especially in vandoids. These observations allow us to further refine character states that are crucial to our understanding of orchid relationships.     

Morphological evolution of Ceratophryinae (Anura, Neobatrachia)

Body form is one of the major consequences of development, and diversification of body shapes implies developmental changes among species. In anurans, changes in the timing of developmental events or heterochrony, have been emphasized as a source of variation in the patterns of development that has lead to diverse morphology. Herein, different approaches are used to explore morphological traits in members of the Ceratophryinae (Anura: Leptodactylidae), a group of frogs with some features produced by overdevelopment. Cladistic analyses were conducted in order to distinguish the shared history of Ceratophrys, Chacophrys and Lepidobatrachus and other anurans. From these studies, morphological variation of selected skeletal features in ceratophryines reveals the presence of ancient structures, which have been considered lost in the neobatrachian phylogeny, integrated in particular designs. Thin-plate spline morphometric analyses of skull shapes among ceratophryines describe Lepidobatrachus as the most distinctive shape. Moreover, thin-plate spline morphometric analyses among anurans show divergent skull shapes between ceratophryines and other anurans, reflecting that the skull shapes of ceratophryines are a result of peramorphosis (increase of developmental rates). This study represents the first detailed examination of the role of peramorphosis in a clade of anurans.