Physiological and metabolic aspects of experimental heterochrony in colonial hydroids

Hydractiniid hydroids display a range of morphological variation from sheet-like to runner-like forms, thus exemplifying the patterns of heterochrony found in many colonial animals. Experimental studies of clonal replicates of a Podocoryne carnea colony demonstrate a relationship between these heterochronic traits and physiological and metabolic factors. While colonies exposed to dilute solutions of 2, 4-dinitrophenol (an uncoupler of oxidative phosphorylation) for 4 hours per day show a strong dose-response relationship between within-colony gastrovascular flow rate and the timing of morphological development, colonies exposed for 20 hours per day fail to show this relationship. Spectrofluorometric measures of redox state suggest that the degree of “loose-coupling” of oxidative phosphorylation is proportional to the exposure time. Thus colonies exposed for 20 hours have significantly diminished ATP production relative to colonies exposed for 4 hours. Two underlying factors may be responsible for the breakdown of the dose-response relationship between flow rate and development: (1) colonies exposed to a high dose of uncoupler for 20 hours per day allocate a larger-than-normal share of their total energy budget into maintaining the minimal flow rate required physiologically, and (2) colonies' redox state has a direct effect on the timing of morphological development. The latter effect is particularly intriguing, given the extensive literature relating “metabolic activity” to development. In general, these results suggest a relationship between energy allocation, metabolism, and development in these hydroids, and these interrelationships may be central to the evolutionary process of heterochrony.     

Evolutionary divergence in life history traits among populations of the Lake Malawi cichlid fish Astatotilapia calliptera

During the early stages of adaptive radiation, populations diverge in life history traits such as egg size and growth rates, in addition to eco‐morphological and behavioral characteristics. However, there are few studies of life history divergence within ongoing adaptive radiations. Here, we studied Astatotilapia calliptera, a maternal mouthbrooding cichlid fish within the Lake Malawi haplochromine radiation. This species occupies a rich diversity of habitats, including the main body of Lake Malawi, as well as peripheral rivers and shallow lakes. We used common garden experiments to test for life history divergence among populations, focussing on clutch size, duration of incubation, egg mass, offspring size, and growth rates. In a first experiment, we found significant differences among populations in average clutch size and egg mass, and larger clutches were associated with smaller eggs. In a second experiment, we found significant differences among populations in brood size, duration of incubation, juvenile length when released, and growth rates. Larger broods were associated with smaller juveniles when released and shorter incubation times. Although juvenile growth rates differed between populations, these were not strongly related to initial size on release. Overall, differences in life history characters among populations were not predicted by major habitat classifications (Lake Malawi or peripheral habitats) or population genetic divergence (microsatellite‐based F_ST). We suggest that the observed patterns are consistent with local selective forces driving the observed patterns of trait divergence. The results provide strong evidence of evolutionary divergence and covariance of life history traits among populations within a radiating cichlid species, highlighting opportunities for further work to identify the processes driving the observed divergence.     

Morphological and temporal variation in early embryogenesis contributes to species divergence in Malawi cichlid fishes

The cichlid fishes comprise the largest extant vertebrate family and are the quintessential example of rapid “explosive” adaptive radiations and phenotypic diversification. Despite low genetic divergence, East African cichlids harbor a spectacular intra- and interspecific morphological diversity, including the hyper-variable, neural crest (NC)-derived traits such as coloration and craniofacial skeleton. Although the genetic and developmental basis of these phenotypes has been investigated, understanding of when, and specifically how early, in ontogeny species-specific differences emerge, remains limited. Since adult traits often originate during embryonic development, the processes of embryogenesis could serve as a potential source of species-specific variation. Consequently, we designed a staging system by which we compare the features of embryogenesis between three Malawi cichlid species—Astatotilapia calliptera, Tropheops sp. ‘mauve’ and Rhamphochromis sp. “chilingali”—representing a wide spectrum of variation in pigmentation and craniofacial morphologies. Our results showed fundamental differences in multiple aspects of embryogenesis that could underlie interspecific divergence in adult adaptive traits. First, we identified variation in the somite number and signatures of temporal variation, or heterochrony, in the rates of somite formation. The heterochrony was also evident within and between species throughout ontogeny, up to the juvenile stages. Finally, the identified interspecific differences in the development of pigmentation and craniofacial cartilages, present at the earliest stages of their overt formation, provide compelling evidence that the species-specific trajectories begin divergence during early embryogenesis, potentially during somitogenesis and NC development. Altogether, our results expand our understanding of fundamental cichlid biology and provide new insights into the developmental origins of vertebrate morphological diversity.     

Evolutionary integration of the frog cranium

Evolutionary integration (covariation) of traits has long fascinated biologists because of its potential to elucidate factors that have shaped morphological evolution. Studies of tetrapod crania have identified patterns of evolutionary integration that reflect functional or developmental interactions among traits, but no studies to date have sampled widely across the species-rich lissamphibian order Anura (frogs). Frogs exhibit a vast range of cranial morphologies, life history strategies, and ecologies. Here, using high-density morphometrics we capture cranial morphology for 172 anuran species, sampling every extant family. We quantify the pattern of evolutionary modularity in the frog skull and compare patterns in taxa with different life history modes. Evolutionary changes across the anuran cranium are highly modular, with a well-integrated “suspensorium” involved in feeding. This pattern is strikingly similar to that identified for caecilian and salamander crania, suggesting replication of patterns of evolutionary integration across Lissamphibia. Surprisingly, possession of a feeding larval stage has no notable influence on cranial integration across frogs. However, late-ossifying bones exhibit higher integration than early-ossifying bones. Finally, anuran cranial modules show diverse morphological disparities, supporting the hypothesis that modular variation allows mosaic evolution of the cranium, but we find no consistent relationship between degree of within-module integration and disparity.     

ACCELERATED EVOLUTION OF LAND SNAILS MANDARINA IN THE OCEANIC BONIN ISLANDS: EVIDENCE FROM MITOCHONDRIAL DNA SEQUENCES

An endemic land snail genus Mandarina of the oceanic Bonin (Ogasawara) Islands shows exceptionally rapid evolution not only of morphological and ecological traits, but of DNA sequence. A phylogenetic relationship based on mitochondrial DNA (mtDNA) sequences suggests that morphological differences equivalent to the differences between families were produced between Mandarina and its ancestor during the Pleistocene. The inferred phylogeny shows that species with similar morphologies and life habitats appeared repeatedly and independently in different lineages and islands at different times. Sequential adaptive radiations occurred in different islands of the Bonin Islands and species occupying arboreal, semiarboreal, and terrestrial habitat arose independently in each island. Because of a close relationship between shell morphology and life habitat, independent evolution of the same life habitat in different islands created species possesing the same shell morphology in different islands and lineages. This rapid evolution produced some incongruences between phylogenetic relationship and species taxonomy. Levels of sequence divergence of mtDNA among the species of Mandarina is extremely high. The maximum level of sequence divergence at 16S and 12S ribosomal RNA sequence within Mandarina are 18.7% and 17.7%, respectively, and this suggests that evolution of mtDNA of Mandarina is extremely rapid, more than 20 times faster than the standard rate in other animals. The present examination reveals that evolution of morphological and ecological traits occurs at extremely high rates in the time of adaptive radiation, especially in fragmented environments.     

Ecological divergence among morphologically and genetically related Asphondylia species (Diptera: Cecidomyiidae), with new life history data for three congeners including the Alpinia fruit gall midge

Ecological data is crucial for determining the degree of reproductive isolation among closely related species, and in identifying the factors that have produced this divergence. We studied life history traits for three Asphondylia (Diptera: Cecidomyiidae) species that induce fruit galls either on Alpinia, Ligustrum or Aucuba, and we compared the traits with those published for three other closely related Japanese Asphondylia species. We found that the six species were significantly differentiated in important life history traits, such as host range, voltinism, lower developmental threshold temperature, thermal constant and diapausing season. The data indicate that divergence in the assessed life history traits evolves before morphological divergence, and such ecological divergence could strengthen isolating barriers among the taxa. We present scenarios on how host range expansion, host plant shift and host organ shift for galling initiate the early stages of speciation. We also highlight the importance of ecological data in identifying cryptic species. Specifically, we confirm that Alpinia intermedia (Zingiberaceae) is not an autumn–spring host of the soybean pod gall midge Asphondylia yushimai based on many differences in the life history traits between the Alpinia fruit gall midge Asphondylia sp. and A. yushimai.     

The role of fecundity and reproductive effort in defining life‐history strategies of North American freshwater mussels

Selection is expected to optimize reproductive investment resulting in characteristic trade‐offs among traits such as brood size, offspring size, somatic maintenance, and lifespan; relative patterns of energy allocation to these functions are important in defining life‐history strategies. Freshwater mussels are a diverse and imperiled component of aquatic ecosystems, but little is known about their life‐history strategies, particularly patterns of fecundity and reproductive effort. Because mussels have an unusual life cycle in which larvae (glochidia) are obligate parasites on fishes, differences in host relationships are expected to influence patterns of reproductive output among species. I investigated fecundity and reproductive effort (RE) and their relationships to other life‐history traits for a taxonomically broad cross section of North American mussel diversity. Annual fecundity of North American mussel species spans nearly four orders of magnitude, ranging from < 2000 to 10 million, but most species have considerably lower fecundity than previous generalizations, which portrayed the group as having uniformly high fecundity (e.g. > 200000). Estimates of RE also were highly variable, ranging among species from 0.06 to 25.4%. Median fecundity and RE differed among phylogenetic groups, but patterns for these two traits differed in several ways. For example, the tribe Anodontini had relatively low median fecundity but had the highest RE of any group. Within and among species, body size was a strong predictor of fecundity and explained a high percentage of variation in fecundity among species. Fecundity showed little relationship to other life‐history traits including glochidial size, lifespan, brooding strategies, or host strategies. The only apparent trade‐off evident among these traits was the extraordinarily high fecundity of Leptodea, Margaritifera, and Truncilla, which may come at a cost of greatly reduced glochidial size; there was no relationship between fecundity and glochidial size for the remaining 61 species in the dataset. In contrast to fecundity, RE showed evidence of a strong trade‐off with lifespan, which was negatively related to RE. The raw number of glochidia produced may be determined primarily by physical and energetic constraints rather than selection for optimal output based on differences in host strategies or other traits. By integrating traits such as body size, glochidial size, and fecundity, RE appears more useful in defining mussel life‐history strategies. Combined with trade‐offs between other traits such as growth, lifespan, and age at maturity, differences in RE among species depict a broad continuum of divergent strategies ranging from strongly r‐selected species (e.g. tribe Anodontini and some Lampsilini) to K‐selected species (e.g. tribes Pleurobemini and Quadrulini; family Margaritiferidae). Future studies of reproductive effort in an environmental and life‐history context will be useful for understanding the explosive radiation of this group of animals in North America and will aid in the development of effective conservation strategies.     

Intraspecific morphological divergence in two Cichlid species from Benin

Selection on morphological traits can vary across the range of species, inducing a mosaic of phenotypes across populations. Intraspecific morphological divergence had been demonstrated for many fish groups inhabiting environments with varying abiotic or biotic selective pressures. Such intraspecific phenotypic variation can have a strong influence on the ecologies of species. In the current study, we examined patterns of intraspecific morphological divergence between two populations of Sarotherodon melanotheron and Coptodon guineensis in Lake Ahémé and Porto-Novo lagoon, Benin. Using multiple morphological traits, we demonstrated intraspecific morphological divergence between Lake Ahémé and Porto-Novo lagoon for these species. However, evidence for parallel divergence was found for these two species, implying a similar response to selective pressures might have been acting on labile traits. In addition, species specific morphological changes observed in the current study might be because of differing responses to similar selective forces or taxon-specific selective forces acting on labile traits. The intraspecific trait divergence demonstrated in the current study suggests several possible selective pressures acting on these populations, yet the cause of this divergence remains unknown and additional studies are required to test these inferences.     

Seasonal variations in body melanism and size of the wolf spider Pardosa astrigera (Araneae: Lycosidae)

Variations in species morphology and life‐history traits strongly correlate with geographic and climatic characteristics. Most studies on morphological variations in animals focus on ectotherms distributed on a large geographic scale across latitudinal and/or altitudinal gradient. However, the morphological variations of spiders living in the same habitats across different seasons have not been reported. In this study, we used the wolf spider, Pardosa astrigera, as a model to determine seasonal differences in adult body size, melanism, fecundity, and egg diameter both in the overwintering and the first generation for 2010 and 2016. The results showed that in 2010, both females and males of the overwintering generation were significantly darker than the first generation. Moreover, the overwintering females were markedly larger and produced more and bigger eggs than the first generation in both 2010 and 2016. Considering the overwintering P. astrigera experiencing low temperature and/or desiccation stress, these results suggest that substantially darker and larger body of the overwintering generation is adaptive to adverse conditions.     

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.     

Morphological evolution in Ceratophryinae frogs (Anura,Neobatrachia): the effects of heterochronic changes during larval development and metamorphosis

Heterochrony produces morphological change with effects in shape, size, and/or timing of developmental events of a trait related to an ancestral ontogeny. This paper analyzes heterochrony during the ontogeny of Ceratophryinae (Ceratophrys, Chacophrys, and Lepidobatrachus), a monophyletic group of South American frogs with larval development, and uses different approaches to explore their morphological evolution: (1) inferences of ancestral ontogenies and heterochronic variation from a cladistic analysis based on 102 morphological larval and adult characters recorded in ten anuran taxa; (2) comparisons of size, morphological variation, and timing (age) of developmental events based on a study of ontogenetic series of ceratophryines, Telmatobius atacamensis, and Pseudis platensis. We found Chacophrys as the basal taxon. Ceratophrys and Lepidobatrachus share most derived larval features resulting from heterochrony. Ceratophryines share high rates of larval development, but differ in rates of postmetamorphic growth. The ontogeny of Lepidobatrachus exhibits peramorphic traits produced by the early onset of metamorphic transformations that are integrated in an unusual larval morphology. This study represents an integrative examination of shape, size, and age variation, and discusses evolutionary patterns of metamorphosis. © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 154 , 752–780.     

CONSERVATION OF MOLECULAR PREPATTERNS DURING THE EVOLUTION OF CUTICLE MORPHOLOGY IN DROSOPHILA LARVAE

We are using patterns of cuticle specialization in Drosophila larvae as models to investigate the molecular, genetic, and developmental bases of morphological evolution. Members of the virilis species group differ markedly from one another in the distribution of hairs on the dorsal surface of first instar larvae. In particular, characteristic bands of hairs cover about 20% of each trunk segment in some species but about 70% in others. These major types do not correlate with recently proposed phylogenetic relationships, suggesting that similar phenotypes have arisen independently in different lineages. The patterns of expression of several genes that control or reflect intrasegmental patterning are indistinguishable in species with very different cuticle morphologies. We conclude that, in this case, morphology probably has evolved via altered response to a conserved molecular prepattern.     

Development of the tectum in Gymnophiones,with comparison to other amphibians

Tectal development in a number of caecilian (Gymnophiona: Amphibia) species was examined and compared with that in frogs and salamanders. The caecilian optic tectum develops along the same rostrocaudal and lateromedial gradients as those of frogs and salamanders. However, differences exist in the time course of development. Our data suggest that, as in salamanders, simplification of morphological complexity in caecilians is due to a retardation or loss of late developmental stages. Differences in the time course of development (heterochrony) among different caecilian species are correlated with phylogenetic history as well as with variation in life histories. The most pronounced differences in development occur between the directly developing Hypogeophis rostratus and all other species examined. In this species, the increase in the degree of morphological complexity is greatly accelerated. J. Morphol. 236:233–246, 1998. © 1998 Wiley-Liss, Inc.     

Comparative demography of commercially important parrotfish species from Micronesia

Fishery‐independent sampling was used to determine growth patterns, life span, mortality rates and timing of maturation and sex change in 12 common parrotfishes (Labridae: tribe Scarinae) from five genera (Calotomus, Cetoscarus, Chlorurus, Hipposcarus and Scarus) in Micronesia. Interspecific variation in life‐history traits was explored using multivariate analysis. All species displayed strong sex‐specific patterns of length‐at‐age among which males reached larger asymptotic lengths. There was a high level of correlation among life‐history traits across species. Relationships between length‐based and age‐based variables were weakest, with a tenuous link between maximum body size and life span. Cluster analysis based on similarities among life‐history traits demonstrated that species were significantly grouped at two major levels. The first grouping was driven by length‐based variables (lengths at maturity and sex change and maximum length) and separated the small‐ and large‐bodied species. Within these, species were grouped by age‐based variables (age at maturity, mortality and life span). Groupings based on demographic and life‐history features were independent of phylogenetic relationships at the given taxonomic level. The results reiterate that body size is an important characteristic differentiating species, but interspecific variation in age‐based traits complicates its use as a life‐history proxy. Detailed life‐history metrics should facilitate future quantitative assessments of vulnerability to overexploitation in multispecies fisheries.     

EVOLUTION OF LEAF FORM IN MARSILEACEOUS FERNS: EVIDENCE FOR HETEROCHRONY

Using an explicit phylogenetic framework, ontogenetic patterns of leaf form are compared among the three genera of marsileaceous ferns ( Marsilea , Regnellidium , and Pilularia ) with the outgroup Asplenium to address the hypothesis that heterochrony played a role in their evolution. We performed a Fourier analysis on a developmental sequence of leaves from individuals of these genera. Principal components analysis of the harmonic coefficients was used to characterize the ontogenetic trajectories of leaf form in a smaller dimensional space. Results of this study suggest that the "evolutionary juvenilization" observed in these leaf sequences is best described using a mixed model of heterochrony (accelerated growth rate and early termination at a simplified leaf form). The later stages of the ancestral, more complex, ontogenetic pattern were lost in Marsileaceae, giving rise to the simplified adult leaves of Marsilea , Regnellidium , and Pilularia . Life-history traits such as ephemeral and uncertain habitats, high reproductive rates, and accelerated maturation, which are typical for marsileaceous ferns, suggest that they may be " r strategists." The evidence for heterochrony presented here illustrates that it has resulted in profound ecological and morphological consequences for the entire life history of Marsileaceae.     

Putting prey back together again: integrating predator-induced behavior,morphology, and life history

The last decade has seen an explosion in the number of studies exploring predator-induced plasticity. Recently, there has been a call for more comprehensive approaches that can identify functional relationships between traits, constraints on phenotypic responses, and the cost and benefits of alternative phenotypes. In this study, we exposed Helisoma trivolvis, a freshwater snail, to a factorial combination of three resource levels and five predator environments (no predator, one or two water bugs, and one or two crayfish) and examined ten traits including behavior, morphology, and life history. Each predator induced a unique suite of behavioral and morphological responses. Snails increased near-surface habitat use with crayfish but not with water bugs. Further, crayfish induced narrow and high shells whereas water bugs induced wide shells and wide apertures. In terms of life history, both predators induced delayed reproduction and greater mass at reproduction. However, crayfish induced a greater delay in reproduction that resulted in reduced fecundity whereas water bugs did not induce differences in fecundity. Resource levels impacted the morphology of H. trivolvis; snails reared with greater resource levels produced higher shells, narrower shells, and wider apertures. Resource levels also impacted snail life history; lower resources caused longer times to reproduction and reduced fecundity. Based on an analysis of phenotypic correlations, the morphological responses to each predator most likely represent phenotypic trade-offs. Snails could either produce invasion-resistant shells for defense against water bugs or crush-resistant shells for defense against crayfish, but not both. Our use of a comprehensive approach to examine the responses of H. trivolvis has provided important information regarding the complexity of phenotypic responses to different environments, the patterns of phenotypic integration across environments, and the potential costs and benefits associated with plastic traits.     

Heterochrony: the Evolution of Development

Heterochrony can be defined as change to the timing or rate of development relative to the ancestor. Because organisms generally change in shape as well as increase in size during their development, any variation to the duration of growth or to the rate of growth of different parts of the organism can cause morphological changes in the descendant form. Heterochrony takes the form of both increased and decreased degrees of development, known as “peramorphosis” and “paedomorphosis,” respectively. These are the morphological consequences of the operation of processes that change the duration of the period of an individual’s growth, either starting or stopping it earlier or later than in the ancestor, or by extending or contracting the period of growth. Heterochrony operates both intra- and interspecifically and is the source of much intraspecific variation. It is often also the cause of sexual dimorphism. Selection of a sequence of species with a specific heterochronic trait can produce evolutionary trends in the form of pera- or paedomorphoclines. Many different life history traits arise from the operation of heterochronic processes, and these may sometimes be the targets of selection rather than morphological features themselves. It has been suggested that some significant steps in evolution, such as the evolution of vertebrates, were engendered by heterochrony. Human evolution was fuelled by heterochrony, with some traits, such as a large brain, being peramorphic, whereas others, such as reduced jaw size, are paedomorphic.     

DIVERGENCE AND GENETIC STRUCTURE IN ADJACENT GRASS POPULATIONS. I. QUANTITATIVE GENETICS

Additive genetic variances and covariances were estimated for life history and morphological traits in two adjacent populations of the grass, Holcus lanatus L. Significant phenotypic differentiation was found between the two populations for four of the 15 morphological attributes measured. Significant differences in genetic architecture were found between the two populations for 11 of the 13 traits for which genetic variance components could be calculated. Estimates of genetic correlations also showed considerable divergence between the populations. The genetic divergence was much larger than would have been anticipated from simple measures of phenotypic differentiation. These results show that, even in plant species with relatively large population sizes, differences in genetic variance-covariance patterns can occur between adjacent populations.     

Taxonomy of phyllophoroid algae: the implications of life history

The Phyllophoraceae Rabenhorst (Gigartinales) is a family that shows a great diversity of life history patterns. The three largest phyllophoroid genera, Ahnfeltia, Gymnogongrus and Phyllophora, all commercial sources of phycocolloids, show the greatest range of life history. Information from life history studies has been of significance to classification of the Phyllophoraceae at the family, generic and specific levels. In the tetrasporophyte of Ahnfeltia plicata, previously known as Porphyrodiscus simulans, tetrasporangia are zonate and borne terminally in small superficial sori in contrast to the chains of cruciate tetrasporangia characteristic of the Phyllophoraceae. A study of reproduction and life history in the type species, A. plicata, from the Atlantic concluded that the unique carposporophyte development, in conjunction with the most primitive pit-plug structure known in the Florideophycidae, justified the proposal of a new family Ahnfeltiaceae Maggs et Pueschel in the Ahnfeltiales Maggs et Pueschel. Most Pacific species of Ahnfeltia are instead phyllophoracean and closely related to Gymnogongrus. Gymnogongrus griffithsiae, the type species, forms tetrasporoblasts whereas the majority form internal cystocarps and have heteromorphic life histories. Proposals to divide the genus by life history type require further detailed morphological and ontogenetic studies of G. griffithsiae. Phyllophora species exhibit at least three different types of life history, tetrasporoblastic, isomorphic and heteromorphic, and this genus could likewise be split along these lines. At the specific level, intraspecific life history variability appears to be related to morphological variation in some species of Gymnogongrus.