RESUMO
Environmental variation often induces plastic responses in organisms that can trigger changes in subsequent generations through non-genetic inheritance mechanisms. Such transgenerational plasticity thus consists of environmentally induced non-random phenotypic modifications that are transmitted through generations. Transgenerational effects may vary according to the sex of the organism experiencing the environmental perturbation, the sex of their descendants or both, but whether they are affected by past sexual selection is unknown. Here, we use experimental evolution on an insect model system to conduct a first test of the involvement of sexual selection history in shaping transgenerational plasticity in the face of rapid environmental change (exposure to pesticide). We manipulated evolutionary history in terms of the intensity of sexual selection for over 80 generations before exposing individuals to the toxicant. We found that sexual selection history constrained adaptation under rapid environmental change. We also detected inter- and transgenerational effects of pesticide exposure in the form of increased fitness and longevity. These cross-generational influences of toxicants were sex dependent (they affected only male descendants), and intergenerational, but not transgenerational, plasticity was modulated by sexual selection history. Our results highlight the complexity of intra-, inter- and transgenerational influences of past selection and environmental stress on phenotypic expression.
Assuntos
Praguicidas , Seleção Sexual , Animais , Masculino , Feminino , Praguicidas/toxicidade , Evolução BiológicaRESUMO
Developmental plasticity allows organisms to adjust life-history traits to varying environmental conditions, which can have concomitant effects across life stages. Many amphibians are suitable model systems to study plasticity because their larvae can adjust growth and differentiation under fluctuating environments. It is unknown, however, whether somatic and gonadal differentiation are equally affected by environmentally induced plasticity or whether their decoupling alters gonadal maturation postmetamorphosis, which may affect fitness. We tested if developmental acceleration in response to warming and desiccation risk results in shifts in gonadal maturation during metamorphosis and postmetamorphic growth in western spadefoot toads (Pelobates cultripes). We found additive effects of increased temperature and desiccation risk on development and growth at metamorphosis, which largely constrained gonadal maturation in metamorphic and postmetamorphic individuals of both sexes. Furthermore, the conditions experienced by larvae incurred sex-specific carryover effects on the gonadal maturation of juveniles 5 months after metamorphosis. In females, high temperature delayed ovarian maturation regardless of the water level. In males, exposure to high temperature and high water levels slightly delayed the testes' maturation. These results highlight the relevance of larval plasticity in the gonadal maturation of species undergoing metamorphosis, which may have implications for population demographics and the evolution of life histories.
Assuntos
Anuros , Dessecação , Humanos , Masculino , Feminino , Animais , Larva , Anuros/fisiologia , Bufonidae , Metamorfose Biológica/fisiologia , ÁguaRESUMO
Alien predators are a major cause of decline and extinction of species worldwide, since native organisms are rarely equipped with specific antipredatory strategies to cope with them. However, phenotypic plasticity and learned predator recognition may help prey populations to survive novel predators. Here we examine geographical variation in the learning ability of larval spadefoot toads (Pelobates cultripes) to recognize invasive predatory crayfish (Procambarus clarkii). We compare the learning-mediated behavioural responses of tadpoles from six populations across two regions in Spain (central and southern), with different histories of exposure to the presence of the invasive species. Two of the populations showed innate recognition of chemical cues from the invasive crayfish, whereas three of them learned to recognize such cues as a threat after conditioning with conspecific alarm cues. Learning abilities did not differ among southern populations, but they did among central populations. We assessed patterns of genetic variation within and among these two regions through microsatellite markers and found low genetic divergence among the southern populations but greater differentiation among the central ones. We hypothesize that similar responses to the invasive crayfish in southern populations may have arisen from a combination of extended historical exposure to this introduced predator (~ 50 y) and higher levels of gene flow, as they inhabit a highly interconnected pond network. In contrast, populations from central Spain show lower connectivity, have been exposed to the invasive crayfish for a shorter period of time, and are more divergent in their plastic responses.
Assuntos
Anuros , Astacoidea , Anuros/genética , Anuros/fisiologia , Comportamento Predatório , Comportamento Animal , Plasticidade Neuronal , Repetições de Microssatélites , Larva/fisiologia , Espanha , Genética PopulacionalRESUMO
Global change exposes wildlife to a variety of environmental stressors and is affecting biodiversity worldwide, with amphibian population declines being at the forefront of the global biodiversity crisis. The use of non-invasive methods to determine the physiological state in response to environmental stressors is therefore an important advance in the field of conservation physiology. The glucocorticoid hormone corticosterone (CORT) is one useful biomarker to assess physiological stress in amphibians, and sampling water-borne (WB) CORT is a novel, non-invasive collection technique. Here, we tested whether WB CORT can serve as a valid proxy of organismal levels of CORT in larvae of the common frog (Rana temporaria). We evaluated the association between tissue and WB CORT levels sampled from the same individuals across ontogenetic stages, ranging from newly hatched larvae to froglets at 10 days after metamorphosis. We also investigated how both tissue and WB CORT change throughout ontogeny. We found that WB CORT is a valid method in pro-metamorphic larvae as values for both methods were highly correlated. In contrast, there was no correlation between tissue and WB CORT in newly hatched, pre-metamorphic larvae, metamorphs or post-metamorphic froglets probably due to ontogenetic changes in respiratory and skin morphology and physiology affecting the transdermal CORT release. Both collection methods consistently revealed a non-linear pattern of ontogenetic change in CORT with a peak at metamorphic climax. Thus, our results indicate that WB CORT sampling is a promising, non-invasive conservation tool for studies on late-stage amphibian larvae. However, we suggest considering that different contexts might affect the reliability of WB CORT and consequently urge future studies to validate this method whenever it is used in new approaches. We conclude proposing some recommendations and perspectives on the use of WB CORT that will aid in broadening its application as a non-invasive tool in amphibian conservation physiology.
RESUMO
Facultative colour change is widespread in the animal kingdom, and has been documented in many distantly related amphibians. However, experimental data testing the extent of facultative colour change, and associated physiological and morphological implications are comparatively scarce. Background matching in the face of spatial and temporal environmental variation is thought to be an important proximate function of colour change in aquatic amphibian larvae. This is particularly relevant for species with long larval periods such as the western spadefoot toad, Pelobates cultripes, whose tadpoles spend up to six months developing in temporary waterbodies with temporally variable vegetation. By rearing tadpoles on different coloured backgrounds, we show that P. cultripes larvae can regulate pigmentation to track fine-grained differences in background brightness, but not hue or saturation. We found that colour change is rapid, reversible, and primarily achieved through changes in the quantity of eumelanin in the skin. We show that this increased eumelanin production and/or maintenance is also correlated with changes in morphology and oxidative stress, with more pigmented tadpoles growing larger tail fins and having an improved redox status.
Assuntos
Antioxidantes , Melaninas , Animais , Larva/fisiologia , Bufonidae , Anuros/fisiologia , PigmentaçãoRESUMO
Microplastics (MP) are an abundant, long-lasting, and widespread type of environmental pollution that is of increasing concern as it might pose a serious threat to ecosystems and species. However, these threats are still largely unknown for amphibians. Here, we used the African clawed frog (Xenopus laevis) as a model species to investigate whether polyethylene MP ingestion affects amphibian growth and development and leads to metabolic changes across two consecutive life stages (larvae and juveniles). Furthermore, we examined whether MP effects were more pronounced at higher rearing temperatures. Larval growth, development, and body condition were recorded, and standard metabolic rate (SMR) and levels of stress hormone (corticosterone, CORT) were measured. We determined variation in size, morphology, and hepatosomatic index in juveniles to identify any potential consequences of MP ingestion across metamorphosis. In both life stages, MP accumulation in the body was assessed. MP ingestion was found to result in sublethal effects on larval growth, development, and metabolism, to lead to allometric carry-over effects on juvenile morphology, and to accumulate in the specimens at both life stages. In larvae, SMR and developmental rate increased in response to MP ingestion; there additionally was a significant interaction of MP ingestion and temperature on development. CORT levels were higher in larvae that ingested MP, except at higher temperature. In juveniles, body was wider, and extremities were longer in animals exposed to MP during the larval stage; a high rearing temperature in combination with MP ingestion counteracted this effect. Our results provide first insights into the effects of MP on amphibians throughout metamorphosis and demonstrate that juvenile amphibians may act as a pathway for MP from freshwater to terrestrial environments. To allow for generalizations across amphibian species, future experiments need to consider the field prevalence and abundance of different MP in amphibians at various life stages.
Assuntos
Anfíbios , Microplásticos , Polietileno , Poluentes Químicos da Água , Animais , Ingestão de Alimentos , Ecossistema , Larva , Plásticos/toxicidade , Polietileno/toxicidade , Poluentes Químicos da Água/análiseRESUMO
Amphibians have undergone important evolutionary transitions in reproductive modes and life-cycles. We compare large-scale macroevolutionary patterns in these transitions across the three major amphibian clades: frogs, salamanders, and caecilians. We analyse matching reproductive and phylogenetic data for 4025 species. We find that having aquatic larvae is ancestral for all three groups and is retained by many extant species (33-44%). The most frequent transitions in each group are to relatively uncommon states: live-bearing in caecilians, paedomorphosis in salamanders, and semi-terrestriality in frogs. All three groups show transitions to more terrestrial reproductive modes, but only in caecilians have these evolved sequentially from most-to-least aquatic. Diversification rates are largely independent of reproductive modes. However, in salamanders direct development accelerates diversification whereas paedomorphosis decreases it. Overall, we find a widespread retention of ancestral modes, decoupling of trait transition rates from patterns of species richness, and the general independence of reproductive modes and diversification.
Assuntos
Estágios do Ciclo de Vida , Reprodução , Animais , Filogenia , Estágios do Ciclo de Vida/genética , Reprodução/genética , Anuros , Urodelos/genéticaRESUMO
Genomic resources for amphibians are still hugely under-represented in vertebrate genomic research, despite being a group of major interest for ecology, evolution and conservation. Amphibians constitute a highly threatened group of vertebrates, present a vast diversity in reproductive modes, are extremely diverse in morphology, occupy most ecoregions of the world, and present the widest range in genome sizes of any major group of vertebrates. We combined Illumina, Nanopore and Hi-C sequencing technologies to assemble a chromosome-level genome sequence for an anuran with a moderate genome size (assembly span 3.09 Gb); Pelobates cultripes, the western spadefoot toad. The genome has an N50 length of 330 Mb with 98.6% of the total sequence length assembled into 14 super scaffolds, and 87.7% complete BUSCO genes. We use published transcriptomic data to provide annotations, identifying 32,684 protein-coding genes. We also reconstruct the P. cultripes phylome and identify 2,527 gene expansions. We contribute the first draft of the genome of the western spadefoot toad, P. cultripes. This species represents a relatively basal lineage in the anuran tree with an interesting ecology and a high degree of developmental plasticity, and thus is an important resource for amphibian genomic research.
Assuntos
Anuros , Cromossomos , Animais , Anuros/genética , Genoma , Genômica , Anotação de Sequência Molecular , FilogeniaRESUMO
African amphibian diversity remains underestimated with many cryptic lineages awaiting formal description. An important hotspot of amphibian diversification is the Guineo-Congolian rainforest in Central Africa, its richness attributable to present day and ancestral range fragmentation through geological barriers, habitat expansion and contraction, and the presence of steep ecological gradients. The charismatic Nectophryne tree toads present an interesting case study for diversification in this region. The two formally described species comprising this genus show nearly identical geographic distributions extending across most of the Guineo-Congolian rainforest, but show little morphological disparity. Both species harbour extensive genetic diversity warranting taxonomic revisions, and interestingly, when comparing the subclades within each, the two species show remarkably parallel diversification histories, both in terms of timing of phylogenetic splits and their geographic distributions. This indicates that common processes may have shaped the evolutionary history of these lineages.
Assuntos
Bufonidae/genética , Filogenia , Filogeografia , Floresta Úmida , Animais , Feminino , MasculinoRESUMO
That hardcoded genomes can manifest as plastic phenotypes responding to environmental perturbations is a fascinating feature of living organisms. How such developmental plasticity is regulated at the molecular level is beginning to be uncovered aided by the development of -omic techniques. Here, we compare the transcriptome-wide responses of two species of spadefoot toads with differing capacity for developmental acceleration of their larvae in the face of a shared environmental risk: pond drying. By comparing gene expression profiles over time and performing cross-species network analyses, we identified orthologues and functional gene pathways whose environmental sensitivity in expression have diverged between species. Genes related to lipid, cholesterol and steroid biosynthesis and metabolism make up most of a module of genes environmentally responsive in one species, but canalized in the other. The evolutionary changes in the regulation of the genes identified through these analyses may have been key in the genetic accommodation of developmental plasticity in this system.
Assuntos
Anuros , Transcriptoma , Animais , Anuros/genética , Evolução Biológica , Larva/genética , FenótipoRESUMO
Amphibian larvae are plastic organisms that can adjust their growth and developmental rates to local environmental conditions. The consequences of such developmental alterations have been studied in detail, both at the phenotypic and physiological levels. While largely unknown, it is of great importance to assess how developmental alterations affect the pigmentation pattern of the resulting metamorphs, because pigmentation is relevant for communication, mate choice, and camouflage and hence influences the overall fitness of the toads. Here we quantify the variation in several aspects of the pigmentation pattern of juvenile spadefoot toads experimentally induced to accelerate their larval development in response to decreased water level. It is known that induced developmental acceleration comes at the cost of reduced size at metamorphosis, higher metabolic rate, and increased oxidative stress. In this study, we show that spadefoot toads undergoing developmental acceleration metamorphosed with a less complex, more homogeneous, darker dorsal pattern consisting of continuous blotches, compared to the more contrasted pattern with segregated blotches and higher fractal dimension in normally developing individuals, and at a smaller size. We also observed a marked effect of population of origin in the complexity of the pigmentation pattern. Complexity of the post-metamorphic dorsal pigmentation could therefore be linked to pre-metamorphic larval growth and development.
Assuntos
Anuros/crescimento & desenvolvimento , Anuros/fisiologia , Larva/enzimologia , Larva/crescimento & desenvolvimento , Larva/fisiologia , Pigmentação/fisiologia , Animais , Larva/metabolismo , Estresse OxidativoRESUMO
Telomere shortening with age has been documented in many organisms, but few studies have reported telomere length measurements in amphibians, and no information is available for growth after metamorphosis, nor in wild populations. We provide both cross-sectional and longitudinal evidence of net telomere attrition with age in a wild amphibian population of natterjack toads (Epidalea calamita). Based on age-estimation by skeletochronology and qPCR telomere length measurements in the framework of an individual-based monitoring programme, we confirmed telomere attrition in recaptured males. Our results support that toads experience telomere attrition throughout their ontogeny, and that most attrition occurs during the first 1-2 years. We did not find associations between telomere length and inbreeding or body condition. Our results on telomere length dynamics under natural conditions confirm telomere shortening with age in amphibians and provide quantification of wide telomere length variation within and among age-classes in a wild breeding population.
Assuntos
Encurtamento do Telômero , Telômero , Animais , Bufonidae , Estudos Transversais , Masculino , Telômero/genéticaRESUMO
Organisms are exposed to multiple environmental factors simultaneously to which they often respond behaviorally, morphologically and/or physiologically. Amphibian larvae are quite plastic and efficiently adjust their phenotype and physiology to the reigning local conditions. Here we tested whether the combination of predator presence and low water pH induces alterations in the morphology and physiology of spadefoot toad tadpoles. We raised Pelobates cultripes tadpoles in the laboratory in water at either pH 4 or 7, and in the presence or absence of caged dragonfly nymphs, and determined their changes in shape through geometric morphometrics to assess whether predator recognition was impaired or not at low pH. We also measured levels of plasma corticosterone, activity of four antioxidant enzymes, as well as markers of oxidative damage and redox status. We found that tadpoles altered their body shape in response to predator cues even at low pH, indicating that predator recognition was not interfered by water acidity and developmental responses were robust even under abiotic stress. Water acidity was associated with increased corticosterone levels in tadpoles, whereas predator presence consistently reduced corticosterone levels. Predator presence was linked to reduced antioxidant enzyme activity, whereas the combination of both factors resulted in negative synergistic effects on lipid peroxidation and the antioxidant capacity of tadpoles. Here we show that tadpoles detect predators even at low pH but that the development of adaptive anti-predatory morphology can magnify physiological imbalances when other stressors co-occur. These results emphasize the need to understand how multiple environmental perturbations can affect animal homeostasis.
Assuntos
Ácidos/toxicidade , Anuros/fisiologia , Corticosterona/sangue , Larva/fisiologia , Comportamento Predatório , Estresse Fisiológico , Poluentes Químicos da Água/toxicidade , Animais , Sinais (Psicologia) , Larva/efeitos dos fármacos , FenótipoRESUMO
Adenoviruses are double-strained DNA viruses found in a great number of vertebrates, including humans. In order to understand their transmission dynamics, it is crucial, even from a human health perspective, to investigate how host traits influence their prevalence. Bats are important reservoirs for adenoviruses, and here we use the results of recent screenings in Western Europe to evaluate the association between characteristic traits of bat species and their probability of hosting adenoviruses, taking into account their phylogenetic relationships. Across species, we found an important phylogenetic component in the presence of adenoviruses and mating strategy as the most determinant factor conditioning the prevalence of adenoviruses across bat species. Contrary to other more stable mating strategies (e.g. harems), swarming could hinder transmission of adenoviruses since this strategy implies that contacts between individuals are too short. Alternatively, bat species with more promiscuous behavior may develop a stronger immune system. Outstandingly high prevalence of adenoviruses was reported for the Iberian species Pipistrellus pygmaeus, P. kuhlii and Nyctalus lasiopterus and we found that in the latter, males were more likely to be infected by adenoviruses than females, due to the immunosuppressing consequence of testosterone during the mating season. As a general trend across species, we found that the number of adenoviruses positive individuals was different across localities and that the difference in prevalence between populations was correlated with their geographic distances for two of the three studied bat species (P. pygmaeus and P.kuhlii). These results increase our knowledge about the transmission mechanisms of adenoviruses.
Assuntos
Infecções por Adenoviridae/veterinária , Adenoviridae/classificação , Adenoviridae/genética , Quirópteros/fisiologia , Quirópteros/virologia , Preferência de Acasalamento Animal , Comportamento Sexual Animal , Adenoviridae/isolamento & purificação , Infecções por Adenoviridae/epidemiologia , Infecções por Adenoviridae/virologia , Animais , Quirópteros/psicologia , Europa (Continente)/epidemiologia , Feminino , Masculino , Filogenia , PrevalênciaRESUMO
Amphibians are highly vulnerable and diverse vertebrates for which we still have modest genomic resources. Amphibian larvae are key components of continental wetlands, where they have strong influences on energy fluxes, nutrient cycling, and community structure. Amphibian larvae are highly sensitive to environmental conditions and can often alter their physiology, behavior and even morphology in response to the local conditions experienced, although we still know relatively little about the transcriptomic changes that enable such plasticity. Here we contribute the larval transcriptomes of two spadefoot toad species with divergent developmental rates and degree of developmental plasticity in response to pond drying.
Assuntos
Anuros/genética , Biomarcadores , Biologia Computacional , Perfilação da Expressão Gênica , Transcriptoma , Animais , Biologia Computacional/métodos , Anotação de Sequência Molecular , Especificidade da EspécieRESUMO
Biodiversity loss is a major challenge. Over the past century, the average rate of vertebrate extinction has been about 100-fold higher than the estimated background rate and population declines continue to increase globally. Birth and death rates determine the pace of population increase or decline, thus driving the expansion or extinction of a species. Design of species conservation policies hence depends on demographic data (e.g., for extinction risk assessments or estimation of harvesting quotas). However, an overview of the accessible data, even for better known taxa, is lacking. Here, we present the Demographic Species Knowledge Index, which classifies the available information for 32,144 (97%) of extant described mammals, birds, reptiles, and amphibians. We show that only 1.3% of the tetrapod species have comprehensive information on birth and death rates. We found no demographic measures, not even crude ones such as maximum life span or typical litter/clutch size, for 65% of threatened tetrapods. More field studies are needed; however, some progress can be made by digitalizing existing knowledge, by imputing data from related species with similar life histories, and by using information from captive populations. We show that data from zoos and aquariums in the Species360 network can significantly improve knowledge for an almost eightfold gain. Assessing the landscape of limited demographic knowledge is essential to prioritize ways to fill data gaps. Such information is urgently needed to implement management strategies to conserve at-risk taxa and to discover new unifying concepts and evolutionary relationships across thousands of tetrapod species.
Assuntos
Biodiversidade , Evolução Biológica , Conservação dos Recursos Naturais , Extinção Biológica , Vertebrados/fisiologia , AnimaisRESUMO
Consequences of human actions like global warming, spread of exotic species or resource consumption are pushing species to extinction. Even species considered to be at low extinction risk often show signs of local declines. Here, we evaluate the impact of eucalypt plantations, the best-known exotic tree species worldwide and its interaction with temperature and predators on amphibian development, growth, antipredator responses and physiology. For this purpose, we applied a fully factorial experiment crossing two types of leaf litter (native oak or eucalypt), two temperatures (15 and 20°C) and presence/absence of native predators. We found that leachates of eucalypt leaf litter reduced amphibian development and growth, compromised their antipredator responses and altered their metabolic rate. Increased temperature itself also posed serious alterations on development, growth, antioxidant ability and the immune status of tadpoles. However, the combined effects of eucalypt leaf litter and increased temperature were additive, not synergistic. Therefore, we show that non-lethal levels of a globally spread disruptor such as leachates from eucalypt leaf litter can seriously impact the life history and physiology of native amphibian populations. This study highlights the need to evaluate the status of wild populations exposed to human activities even if not at an obvious immediate risk of extinction, based on reliable stress markers, in order to anticipate demographic declines that may be hard to reverse once started. Replacing eucalypt plantations with native trees in protected areas would help improving the health of local amphibian larvae. In zones of economic interest, we would recommend providing patches of native vegetation around ponds and removing eucalypt leaf litter from pond basins during their dry phase.
RESUMO
The evolution and great diversity of genome size has been of long-standing interest to biologists, but has seldom been investigated on a broad phylogenetic scale. Here we present a comparative quantitative analysis of factors shaping genome size evolution in amphibians, the extant class of vertebrates with the largest variation in genome size. We find that amphibian genomes have undergone saltations in size, although these are rare and the evolutionary history of genome size in amphibians has otherwise been one of gradual, time-dependent variation (that is, Brownian motion). This macroevolutionary homogeneity is remarkable given the evolutionary and ecological diversity of most other aspects of the natural history of amphibians. Contrary to previous claims, we find no evidence for associations between life cycle complexity and genome size despite the high diversity of reproductive modes and the multiple events of independent evolution of divergent life cycles in the group. Climate (temperature and humidity) affects genome size indirectly, at least in frogs, as a consequence of its effect on premetamorphic developmental period, although directionality of the relationship between developmental period and genome size is not unequivocal.
Assuntos
Anuros/fisiologia , Evolução Biológica , Clima , Genoma , Características de História de Vida , Animais , Anuros/genética , Evolução MolecularRESUMO
Phenotypic differences among species may evolve through genetic accommodation, but mechanisms accounting for this process are poorly understood. Here we compare hormonal variation underlying differences in the timing of metamorphosis among three spadefoot toads with different larval periods and responsiveness to pond drying. We find that, in response to pond drying, Pelobates cultripes and Spea multiplicata accelerate metamorphosis, increase standard metabolic rate (SMR), and elevate whole-body content of thyroid hormone (the primary morphogen controlling metamorphosis) and corticosterone (a stress hormone acting synergistically with thyroid hormone to accelerate metamorphosis). In contrast, Scaphiopus couchii has the shortest larval period, highest whole-body thyroid hormone and corticosterone content, and highest SMR, and these trait values are least affected by pond drying among the three species. Our findings support that the atypically rapid and canalized development of S. couchii evolved by genetic accommodation of endocrine pathways controlling metamorphosis, showing how phenotypic plasticity within species may evolve into trait variation among species.
Assuntos
Anuros/genética , Anuros/metabolismo , Biodiversidade , Corticosterona/metabolismo , Metamorfose Biológica/fisiologia , Locos de Características Quantitativas , Hormônios Tireóideos/metabolismo , Animais , Anuros/classificação , Anuros/crescimento & desenvolvimento , Evolução Biológica , Desidratação , Larva/metabolismo , Fenótipo , Lagoas , Transdução de SinaisRESUMO
It can be challenging for organisms to achieve a good match between their phenotypic characteristics and environmental requirements that vary in space and time. The evolution of adaptive phenotypes can result from genetic differentiation at the population level. Individuals, however, could also change their phenotype (adaptive plasticity) or select an environment because it matches with their phenotype (matching habitat choice). It is poorly known under which conditions these different solutions to environmental heterogeneity evolve and whether they operate together. Using an individual-based simulation model, we assessed which solutions evolved depending on degree of temporal variation, costs of multiple underlying traits, and order of dispersal and development. Population genetic divergence was superseded by plasticity or matching habitat choice as temporal variation increased. Plasticity and matching habitat choice were limited by their trait costs, even when this involved only a part of the underlying traits. Independent of the order of dispersal and development, plasticity evolved more commonly than matching habitat choice, in part because the match a phenotype can achieve by matching habitat choice is limited by the types of environments available. Our results explain the apparent relative rarity of matching habitat choice in nature. At the same time, our results can be used to look for matching habitat choice in those biological systems where the conditions for other solutions seem unfavorable.