Ecological and evolutionary genetics of Arabidopsis

The crucifer Arabidopsis thaliana has been the subject of intense research into molecular and developmental genetics. One of the consequences of having this wealth of physiological and molecular data available, is that ecologists and evolutionary biologists have begun to incorporate this model system into their studies. Current research on A. thaliana and its close relatives ably illustrates the potential for synergy between mechanistic and organismal biology. On the one hand, mechanistically oriented research can be placed in an historical context, which takes into account the particular phylogenetic history and ecology of these species. This helps us to make sense of redundancies, anomalies and sub-optimalities that would otherwise be difficult to interpret. On the other hand, ecologists and evolutionary biologists now have the opportunity to investigate the physiological and molecular basis for the phenotypic changes they observe. This provides new insight into the mechanisms that influence evolutionary change.     

The role of ethics in experimental marine biology and ecology

Although most countries have ethical guidelines for research involving human subjects and other sentient animals, the ethical issues associated with field research have received little attention. Most experimental marine biologists and ecologists operate without ethical guidelines or scrutiny, despite intermittent community concern about their activities. We offer suggestions on how marine biologists and ecologists can protect the future of research involving the field collection and experimental manipulation of organisms by developing mechanisms to address community concerns that such research is ethically responsible. We urge experimental marine biologists and ecologists to take pre-emptive initiatives by encouraging: (1) institutional animal ethics committees to broaden their terms of reference to include environmental ethics; (2) scientific societies to develop codes of ethics to guide the environmental research conducted by their members; (3) editorial boards of journals to require the research they publish to conform to an appropriate code of ethics, and (4) management agencies that issue permits for field research to establish an ethics committee to advise them on the ethical issues raised by specific research proposals. We conclude that the resultant administrative burden on scientists would be low but that the penalties of operating without such protection can be high.     

Coping with multiple enemies: an integration of molecular and ecological perspectives

How plants respond to attack by the range of herbivores and pathogens that confront them in the field is the subject of considerable research by both molecular biologists and ecologists. However, in spite of the shared focus of these two bodies of research, there has been little integration between them. We consider the scope for such integration, and how greater dialogue between molecular biologists and ecologists could advance understanding of plant responses to multiple enemies.     

The genetic basis of altitudinal variation in the wood frog Rana sylvatica II. An experimental analysis of larval development

Summary The variation in larval developmental patterns in the wood frog, Rana sylvatica, along an elevation gradient of 1,000 m was experimentally studied. Larval populations at high elevation ponds had lower growth rates, developmental rates and were larger at all stages (including metamorphic climax) than larval populations developing in low elevation ponds. There was considerable variation among ponds within each elevation in both the length of the larval period and size at metamorphic climax. Reciprocal transplant experiments and controlled laboratory experiments revealed that most of the observed variation between high and low elevation populations could be explained by the effects of temperature induction during ontogeny. Significant genetic differences in growth rates and non-genetic maternal effects on developmental rates between larvae of mountain origin and lowland origin were also demonstrated. Selection in both environments has acted to minimize the prevailing environmental effect of pond temperature on developmental rates, but has accentuated the prevailing environmental effects on larval body size. As a consequence mountain larvae were capable of completing metamorphosis sooner and at a larger size in all environments than lowland larvae.     

Local adaptation for enhanced salt tolerance reduces non‐adaptive plasticity caused by osmotic stress

Organisms often respond to environmental change via phenotypic plasticity, in which an individual modulates its phenotype according to the environment. Highly variable or changing environments can exceed physiological limits and generate maladapted plastic phenotypes, which is termed nonadaptive plasticity. In some cases, selection may reduce the negative or disruptive impacts of environmental stress and produce locally adapted populations. Salt is an increasingly prevalent contaminant of freshwater systems and can induce nonadaptive plastic phenotypes for freshwater organisms like amphibians. Hyla cinerea is a frog species with populations inhabiting brackish, coastal habitats, so we use this species to test whether coastal populations are locally adapted to tolerate saltwater by determining how salt exposure during the embryonic and larval stages alters mortality and plastic developmental and metamorphic phenotypes of coastal and inland populations. Coastal frogs have higher survival, faster growth rates, and metamorphose sooner than inland frogs across salinities. Coastal frogs also metamorphose smaller (likely a consequence of earlier metamorphosis) yet maintain constant size, while higher salinities reduce metamorphic size for inland frogs. Coastal frogs evolved to minimize nonadaptive and disruptive impacts of saltwater during larval development and accelerate the larval period to reduce time spent in a stressful environment.     

Altered thyroid hormone levels affect the capacity for temperature-induced developmental plasticity in larvae of Rana temporaria and Xenopus laevis

Anuran larvae show phenotypic plasticity in age and size at metamorphosis as a response to temperature variation. The capacity for temperature-induced developmental plasticity is determined by the thermal adaptation of a population. Multiple factors such as physiological responses to changing environmental conditions, however, might influence this capacity as well. In anuran larvae, thyroid hormone (TH) levels control growth and developmental rate and changes in TH status are a well-known stress response to sub-optimal environmental conditions. We investigated how chemically altered TH levels affect the capacity to exhibit temperature-induced developmental plasticity in larvae of the African clawed frog (Xenopus laevis) and the common frog (Rana temporaria). In both species, TH level influenced growth and developmental rate and modified the capacity for temperature-induced developmental plasticity. High TH levels reduced thermal sensitivity of metamorphic traits up to 57% (R. temporaria) and 36% (X. laevis). Rates of growth and development were more plastic in response to temperature in X. laevis (+30%) than in R. temporaria (+6%). Plasticity in rates of growth and development is beneficial to larvae in heterogeneous habitats as it allows a more rapid transition into the juvenile stage where rates of mortality are lower. Therefore, environmental stressors that increase endogenous TH levels and reduce temperature-dependent plasticity may increase risks and the vulnerability of anuran larvae. As TH status also influences metabolism, future studies should investigate whether reductions in physiological plasticity also increases the vulnerability of tadpoles to global change.     

Metamorphic Changes in Glycolipids and Myelin Proteins and 2',3'-Cyclic Nucleotide 3'-Phosphohydrolase in Bullfrog and Axolotl Brains

Abstract: The metamorphic changes in levels of glycolipids and myelin proteins and 2',3'-cyclic nucleotide 3'-phosphohydrolase (CNP) in the brains of bullfrog tadpoles, adult frogs, and axolotls were investigated, with particular emphasis on myelin maturation. The concentrations of cerebroside. sulfatide, and galactosyldiacylglycerol gradually increased from the onset of prometamorphosis throughout the active metamorphic period and then greatly increased after metamorphosis was completed. The ratio of glucocerebroside to galactocerebroside increased greatly in the prometamorphic period and then rapidly decreased to the frog level during the climax period. The fatty acid compositions of cerebroside and sulfatide showed a developmental change, with 24:1 being more predominant in the later metamorphic stage. The proportion of hydroxy fatty acids increased up to the onset of the prometamorphic stage and thereafter remained constant at ∼ 50% of the total. The CNP activity remained unchanged throughout metamorphosis at 60% that in frog myelin and increased in the adult frog. The composition of tadpole myelin proteins remained constant during metamorphosis, with large basic protein being the most abundant, and in the frog, proteolipid protein and large basic protein were present in comparable amounts. The two adult forms of axolotl, i.e., the neotenous and metamorphosed forms, exhibited almost identical myelin constituents, and CNP activity in the neotenous form amounted to one-fifth that in the bullfrog. These results indicate that active biosynthesis of myelin marker components occurs as metamorphosis proceeds, but more pronounced changes of myelin components occur after metamorphosis is completed.     

Behavioral plasticity mitigates risk across environments and predators during anuran metamorphosis

Most animals metamorphose, changing morphology, physiology, behavior and ecological interactions. Size- and habitat-dependent mortality risk is thought to affect the evolution and plastic expression of metamorphic timing, and high predation during the morphological transition is posited as a critical selective force shaping complex life cycles. Nonetheless, empirical data on how risk changes across metamorphosis and stage-specific habitats, or how that varies with size, are rare. We examined predator–prey interactions of red-eyed treefrogs, Agalychnis callidryas, with an aquatic predator (giant water bug, Belostoma) and a semi-terrestrial predator (fishing spider, Thaumasia) across metamorphosis. We manipulated tadpole density to generate variation in metamorph size and conducted predation trials at multiple developmental stages. We quantified how frog behavior (activity) changes across metamorphic development, habitats, and predator presence or absence. In aquatic trials with water bugs, frog mortality increased with forelimb emergence, as hypothesized. In semi-terrestrial trials, contrary to predictions, predation by spiders increased, not decreased, with tail resorption. In neither case did frog size affect mortality. Frogs reduced activity upon forelimb emergence in the water, and further with emergence into air, then increased activity with tail resorption. Longer-tailed metamorphs were captured more often in spider attacks, but attacked less, as most attacks followed prey movements. Metamorphs behaviorally compensated for poor escape performance more effectively on land than in water, thus emergence timing may critically affect mortality. The developmental timing of the ecological transition between environments that select for different larval and juvenile phenotypes is an important, neglected variable in studies of complex life cycles.     

Reproductive fitness consequences of progenesis: Sex‐specific pay‐offs in safe and risky environments

Progenesis is considered to have an important role in evolution because it allows the retention of both a larval body size and shape in an adult morphology. However, the cost caused by the adoption of a progenetic process in both males and females remains to be explored to explain the success of progenesis and particularly its biased prevalence across the sexes and environments. Here, through an experimental approach, we used a facultative progenetic species, the palmate newt (Lissotriton helveticus) that can either mature at a small size and retain gills or mature after metamorphosis, to test three hypotheses for sex‐specific pay‐offs of progenesis in safe versus risky habitats. Goldfish were used because they caused a higher decline in progenetic than metamorphic newts. We determined that progenetic newts have a lower reproductive fitness than metamorphic newts. We also found that, when compared to metamorphs, progenetic males have lower reproductive activity than progenetic females and that predatory risk affects more progenetic than metamorphic newts. By identifying ultimate causes of the female‐biased sex ratios found in nature, these results support the male escape hypothesis, that is the higher metamorphosis rate of progenetic males. They also highlight that although progenesis is advantageous in advancing the age at first reproduction, it also brings an immediate fitness cost and this, particularly, in hostile predatory environments. This means that whereas some environmental constraints could favour facultative progenesis, some others, such as predation, can ultimately counter‐select progenesis. Altogether, these results improve our understanding of how developmental processes can affect the sexes differently and how species invasions can impair the success of alternative developmental phenotypes.     

Inferring Predator Behavior from Attack Rates on Prey-Replicas That Differ in Conspicuousness

Behavioral ecologists and evolutionary biologists have long studied how predators respond to prey items novel in color and pattern. Because a predatory response is influenced by both the predator’s ability to detect the prey and a post-detection behavioral response, variation among prey types in conspicuousness may confound inference about post-prey-detection predator behavior. That is, a relatively high attack rate on a given prey type may result primarily from enhanced conspicuousness and not predators’ direct preference for that prey. Few studies, however, account for such variation in conspicuousness. In a field experiment, we measured predation rates on clay replicas of two aposematic forms of the poison dart frog Dendrobates pumilio, one novel and one familiar, and two cryptic controls. To ask whether predators prefer or avoid a novel aposematic prey form independently of conspicuousness differences among replicas, we first modeled the visual system of a typical avian predator. Then, we used this model to estimate replica contrast against a leaf litter background to test whether variation in contrast alone could explain variation in predator attack rate. We found that absolute predation rates did not differ among color forms. Predation rates relative to conspicuousness did, however, deviate significantly from expectation, suggesting that predators do make post-detection decisions to avoid or attack a given prey type. The direction of this deviation from expectation, though, depended on assumptions we made about how avian predators discriminate objects from the visual background. Our results show that it is important to account for prey conspicuousness when investigating predator behavior and also that existing models of predator visual systems need to be refined.     

Ontogeny of the Thyroid Glands During Larval Development of South American Horned Frogs (Anura,Ceratophryidae)

The role of thyroid hormone (TH) in anuran metamorphosis has been documented from a variety of approaches, but the sequence of morpho-histological development of the thyroid glands that produce the secretion of the hormone was assumed invariant from studies of relatively few species even when the effects of environmental influences on larval development and metamorphosis have been largely documented. There are anurans in which developmental and growth rates diverge, and the resulting heterochrony in growth and development produces giant/miniature tadpoles, and or rapid/delayed metamorphosis suggesting changes of the activity of the thyroid glands during larval development. Herein, we analyze the morpho-histological variation of the thyroid glands in larval series of Ceratophrys cranwelli, Chacophrys pierottii, Lepidobatrachus laevis and L. llanensis that share breeding sites along semiarid environments of the Chaco in South America, belong to a monophyletic lineage, and present accelerated patterns in growth and development in order to have a morphological evidence about a possible shift of TH physiology. We describe gross morphology and histology of the thyroid glands and find features shared by all studied species such as the presence of supernumerary heterotopic follicles; changes in the volume and number of follicles towards the metamorphic climax, and cuboidal epithelia with occasional intra-cellular vacuoles as signs of low glandular activity without a manifest peak at the climax as it was assumed for anurans. We discuss different lines of evidence to interpret sources of extra supplement of TH to support the rapid metamorphosis. These interpretations highlight the necessity to design a research program to investigate the endocrine variation during development of ceratophryids taking in account their morphology, physiology and ecology in order to learn more about the effects of environmental and developmental interactions involved in the anuran evolution.     

Getting out alive: how predators affect the decision to metamorphose

Metamorphosis has intrigued biologists for a long time as an extreme form of complex life cycles that are ubiquitous in animals. While investigated from a variety of perspectives, the ecological focus has been on identifying and understanding the ecological factors that affect an individual’s decision on when, and at what size, to metamorphose. Predation is a major factor that affects metamorphic decisions and a recent review by Benard (Annu Rev Ecol Evol Syst 35:651–673, 2004)) documented how predator cues induce metamorphic changes relative to model predictions. Importantly, however, real predators affect larval prey via several mechanisms beyond simple induction. In this paper, I contrast the leading models of metamorphosis, provide an overview of the multiple ways that predators can directly and indirectly affect larval growth and development (via induction, thinning, and selection), and identify how each process should affect the time to and size at metamorphosis. With this mechanistic foundation established, I then turn to the well-studied model system of larval amphibians to synthesize studies on: (1) caged predators (which cause only induction), and (2) lethal predators (which cause induction, thinning, and selection). Among the caged-predator studies, the chemical cues emitted by predators rarely induce a smaller size at metamorphosis or a shorter time to metamorphosis, which is in direct contrast to theoretical predictions but in agreement with Benard’s (Annu Rev Ecol Evol Syst 35:651–673, 2004) review based on a considerably smaller dataset. Among the lethal-predator studies, there is a diversity of outcomes depending upon the relative importance of induction versus thinning with the relative importance of the two processes appearing to change with larval density. Finally, I review the persistent effects of larval predators after metamorphosis including both phenotypic and fitness effects. At the end, I outline a number of future directions to allow researchers to continue gaining insight into how predators affect the metamorphic decisions of their prey. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Heterochrony during skeletal development of Pseudis platensis (anura,hylidae) and the early offset of skeleton development and growth

The aquatic frog Pseudis platensis has a giant tadpole, long developmental time, and dissociated metamorphic events that include later offset of larval somatic morphologies. Moreover, when the tadpole metamorphoses, the young frog is nearly the size of an adult, suggesting that this species has low rates of postmetamorphic growth. Herein, we study the development of the skeleton during larval development up to the end of metamorphosis, which is denoted by the complete lost of the tail in P. platensis. Our study revealed heterochronic differences in skeletal development compared with that of most anurans; these involve the complete differentiation of skull bones and the extensive ossification of the postcranial skeleton before completion of metamorphosis. The skull of metamorphosing P. platensis has an ossified sphenethmoid and a fully formed plectral apparatus, thus differing with regard to the pattern observed in most anurans in which both developmental events take place during the postmetamorphic life. Despite the fact that the iliosacral articulation and the urostyle are present at the end of metamorphosis as in most anurans, ossification/calcification of carpus, tarsus, and limb epihyses during metamorphosis of P. platensis suggests that the postcranial skeleton lacks postmetamorphic growth. This study also includes a discussion of the pattern of development of the plectral apparatus, which allows us to propose a new hypothesis regarding pars externa plectri homology. J. Morphol., 2009. © 2008 Wiley‐Liss, Inc.     

Genetic variability predicts common frog (Rana temporaria) size at metamorphosis in the wild

We investigated associations between genetic variability and two fitness-related traits--size and age at metamorphosis--in two subartic populations of the common frog, Rana temporaria. We found that metamorphic size was positively correlated with individual heterozygosity (as estimated using eight microsatellite loci) and that maternal heterozygosity also explained a significant amount of variation in this trait. In contrast, age at metamorphosis was only explained by environmental factors. Since size at metamorphosis is positively correlated with fitness in amphibians, these results suggest that genetic variability may be an important component of individual fitness in common frogs. The environmental variation underlying timing of metamorphosis may indicate that strong selection pressure on this trait in the Nordic environment is likely to override genetic effects.     

Metamorphic duration: an under-studied variable in frog life histories

Over a narrow temperature range (25.5–28 °C), metamorphic duration in 14 taxonomically diverse frog species ranged from 2.0 to 7.3 days. For 12 species, duration was significantly related to tadpole body-size parameters, especially tail length. For the remainder, duration was longer than expected. Two patterns of tail regression were seen with either rapid or slow regression at the start. Most species lost about 30% of body wet weight during metamorphosis, but two were exceptional: X. laevis lost 58% and F. fitzgeraldi 13%. The results are discussed in the context of Wassersug & Sperry's (1977 ) hypothesis that selection acts to minimize metamorphic duration because metamorphosis is a highly vulnerable stage. Several other factors are outlined as possible determinants of metamorphic duration: developmental constraints, functional trade-offs, phylogeny, predator abundance, adaptive de-coupling, body condition and metabolic and water costs. There is evidence from the data for the operation of several of these factors, especially in species utilizing specialized habitats, and a plea is made for further study of metamorphic duration as an ecologically and evolutionarily important variable in amphibian life histories. Finally, the effects of different temperatures on metamorphic duration are presented for several species, and discussed in terms of local adaptation and reaction norms.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 83 , 261–272.     

Plethodontid salamanders do not conform to "general rules" for ectotherm life histories: insights from allocation models about why simple models do not make accurate predictions

Recent theoretical models hold that temperature imposes unalterable physiological effects on ectotherm growth and development such that their life histories are dictated by local biophysical environments. Models relying on this premise have been offered to explain many life history phenotypes including threshold traits such as age/size at metamorphosis/maturity. Because threshold traits are thought to influence adult fitness components by affecting performance of an individual in its new habitat, they are evolutionarily important components of complex life cycles. Consequently, the ecological and genetical basis of variation in such traits has been the focus of a large research program by evolutionary biologists, and amphibians have been model systems for these studies in the last three decades. Smith‐Gill and Berven proposed a physiological model to explain commonly observed clinal patterns of variation in metamorphosis, and it appears to account successfully for patterns observed in a few species of pond‐breeding frogs and salamanders (Rana and Ambystoma). However, six species of stream‐breeding salamanders (family Plethodontidae: Desmognathus, Pseudotriton, Eurycea) contradict both the phenotypic patterns found in nature for pond‐breeding species as well as the predictions of this model. Four of the six species of plethodontids have significantly larger metamorphs at lower, warmer elevations (or more southerly latitudes) rather than at higher, cooler sites; two species show no clinal pattern. In light of these results, we critically examine the assumptions of and support for SGB. We propose alternative hypotheses to explain patterns of variation in metamorphic traits along thermal gradients, focusing on a) differences between pond‐breeding Amphibia and plethodontids in basic biology and larval habitats, b) gradients in other biotic and abiotic factors, and c) other effects of temperature on organismal function. Finally, we discuss our results in the context of current models of how ectotherm life histories are affected by temperature.     

Eco-evolutionary dynamics

Evolutionary ecologists and population biologists have recently considered that ecological and evolutionary changes are intimately linked and can occur on the same time-scale. Recent theoretical developments have shown how the feedback between ecological and evolutionary dynamics can be linked, and there are now empirical demonstrations showing that ecological change can lead to rapid evolutionary change. We also have evidence that microevolutionary change can leave an ecological signature. We are at a stage where the integration of ecology and evolution is a necessary step towards major advances in our understanding of the processes that shape and maintain biodiversity. This special feature about ‘eco-evolutionary dynamics’ brings together biologists from empirical and theoretical backgrounds to bridge the gap between ecology and evolution and provide a series of contributions aimed at quantifying the interactions between these fundamental processes.