Experimentally induced life-history evolution in a killifish in response to the introduction of guppies

Life-history theory predicts that increased predation on juvenile age/size-classes favors delayed maturation and decreased reproductive investment. Although this theory has received correlative support, experimental tests in nature are rare. In 1976 and 1981, guppies (Poecilia reticulata) were transplanted into localities that previously only contained a killifish, Rivulus hartii. This situation presents an opportunity to experimentally test this life-history prediction because guppies prey upon young Rivulus. We evaluated the response to selection in Rivulus by measuring phenotypic and genotypic divergence between introduction and upstream "control" localities that lack guppies. Contrary to expectations, Rivulus from the introduction sites evolved earlier maturation and increased reproductive investment within 25 years. Such evolutionary changes parallel previous investigations on natural communities of Rivulus, but do not comply with predictions of age/size-specific theory. Guppies also caused reduced densities and increased growth rates of Rivulus, which are hypothesized indirect effects of predation. Additional life-history theories show that changes in density and growth can interact with predator-induced mortality to alter the predicted trajectory of evolution. We discuss how these latter frameworks improve the fit between theory and evolution in Rivulus.     

Body size variation and caste ratios in geographically distinct populations of the invasive big‐headed ant,Pheidole megacephala (Hymenoptera: Formicidae)

Body size is an important life history trait that can evolve rapidly as a result of how species interact with each other and their environment. Invasive species often encounter vastly different ecological conditions throughout their introduced range that can influence relative investment in growth, reproduction and defence among populations. In this study, we quantified variation in worker size, morphology and proportion of majors among five populations of a worldwide invasive species, the big‐headed ant, Pheidole megacephala (Fabricius). The sampled populations differed in ant community composition, allowing us to examine if P. megacephala invests differently in the size and number of majors based on the local ant fauna. We also used genetic data to determine if these populations of P. megacephala represented cryptic species or if morphological differences could be attributed to change following introduction. We found significant variation in worker mass among the populations. Both major and minor workers were largest in Australia, where the ant fauna was most diverse, and minor workers were smallest in Hawaii and Mauritius, where P. megacephala interacted with few to no other ants. We also found differences in major and minor worker morphology among populations. Majors from Mauritius had significantly larger heads (width and length) relative to whole body size than those from Hawaii and Florida. Minors had longer heads and hind tibias in South Africa compared with populations from Australia, Hawaii and Florida. The proportion of majors did not differ among populations, suggesting that these populations may not be subject to trade‐offs in investment in major size versus number. Our molecular data place all samples within the same clade, supporting that these morphologically different populations represent the same species. These results suggest that the variation in shape and morphology of major and minor workers may therefore be the result of rapid adaptation or plastic responses to local conditions. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 423–438.     

Adaptation to developmental diet influences the response to selection on age at reproduction in the fruit fly

Experimental evolution (EE) is a powerful tool for addressing how environmental factors influence life‐history evolution. While in nature different selection pressures experienced across the lifespan shape life histories, EE studies typically apply selection pressures one at a time. Here, we assess the consequences of adaptation to three different developmental diets in combination with classical selection for early or late reproduction in the fruit fly Drosophila melanogaster. We find that the response to each selection pressure is similar to that observed when they are applied independently, but the overall magnitude of the response depends on the selection regime experienced in the other life stage. For example, adaptation to increased age at reproduction increased lifespan across all diets; however, the extent of the increase was dependent on the dietary selection regime. Similarly, adaptation to a lower calorie developmental diet led to faster development and decreased adult weight, but the magnitude of the response was dependent on the age‐at‐reproduction selection regime. Given that multiple selection pressures are prevalent in nature, our findings suggest that trade‐offs should be considered not only among traits within an organism, but also among adaptive responses to different—sometimes conflicting—selection pressures, including across life stages.     

Short‐term larval food stress and associated compensatory growth reduce adult immune function in a damselfly

Abstract 1. In animals with a complex life cycle, larval stressors may carry over to the adult stage. Carry‐over effects not mediated through age and size at metamorphosis have rarely been studied. The present study focuses on the poorly documented immune costs of short‐term food stress both in the larval stage and after metamorphosis in the adult stage. 2. The present study quantified immune function [number of haemocytes, activity of prophenoloxidase (proPO) and phenoloxidase (PO)] in an experiment where larvae of the damselfly Lestes viridis were exposed to a transient starvation period. 3. Directly after starvation, immune variables were reduced in starved larvae. Levels of proPO and PO remained low after starvation, even after metamorphosis. In contrast, haemocyte numbers were fully compensated by the end of the larval stage, yet were lower in previously starved animals after metamorphosis. This can be explained as a cost of the observed compensatory growth after starvation. Focusing only on potential costs of larval stressors within the larval stage may therefore be misleading. 4. The here‐identified immunological cost in the adult stage of larval short‐term food stress and associated compensatory growth strongly indicates that physiological costs may explain hidden carry‐over effects bridging metamorphosis. This adds to the increasing awareness that the larval and adult stages in animals with a complex life cycle should be jointly studied, as trade‐offs may span metamorphosis.     

One stimulus—Two responses: Host and parasite life‐history variation in response to environmental stress

Climate change stressors will place different selective pressures on both parasites and their hosts, forcing individuals to modify their life‐history strategies and altering the distribution and prevalence of disease. Few studies have investigated whether parasites are able to respond to host stress and respond by varying their reproductive schedules. Additionally, multiple environmental stressors can limit the ability of a host to respond adaptively to parasite infection. This study compared both host and parasite life‐history parameters in unstressed and drought‐stressed environments using the human parasite, Schistosoma mansoni, in its freshwater snail intermediate host. Snail hosts infected with the parasite demonstrated a significant reproductive burst during the prepatent period (fecundity compensation), but that response was absent in a drought‐stressed environment. This is the first report of the elimination of host fecundity compensation to parasitism when exposed to additional environmental stress. More surprisingly, we found that infections in drought‐stressed snails had significantly higher parasite reproductive outputs than infections in unstressed snails. The finding suggests that climate change may alter the infection dynamics of this human parasite.     

Personality‐related differences in response to habitat in Mediterranean blue tits

Habitat‐specific selection pressures have been widely recognized, but whether selection favours different personality types in different habitats has rarely been evaluated. This study aimed to test whether personality‐related differences in annual reproductive success differed between two populations of blue tits (Cyanistes caeruleus) occupying different Mediterranean habitats (oakwood and pinewood). We measured exploration and parental provisioning behaviours and used a path analysis to ask how the interplay between these two behavioural traits affected reproductive success in each of these two habitats. We found that blue tits breeding in the pinewood were slow‐exploring compared to blue tits breeding in the oakwood, suggesting the occurrence of personality‐related differences in settlement, or behavioural plasticity in response to habitat. Exploration behaviour and feeding rates were positively associated, suggesting that they affect each other or that there is an environmental factor affecting both traits simultaneously. Finally, fast explorers were favoured in the pinewood, while there was no selection acting on exploration behaviour in the oak habitat. These findings emphasize the importance of integrating habitat selection, plasticity and personality in the study of behavioural evolution.     

Within-population variation in body size plasticity in response to combined nutritional and thermal stress is partially independent from variation in development time

Ongoing climate change has forced animals to face changing thermal and nutritional environments. Animals can adjust to such combinations of stressors via plasticity. Body size is a key trait influencing organismal fitness, and plasticity in this trait in response to nutritional and thermal conditions varies among genetically diverse, locally adapted populations. The standing genetic variation within a population can also influence the extent of body size plasticity. We generated near-isogenic lines from a newly collected population of Drosophila melanogaster at the mid-point of east coast Australia and assayed body size for all lines in combinations of thermal and nutritional stress. We found that isogenic lines showed distinct underlying patterns of body size plasticity in response to temperature and nutrition that were often different from the overall population response. We then tested whether plasticity in development time could explain, and therefore regulate, variation in body size to these combinations of environmental conditions. We selected five genotypes that showed the greatest variation in response to combined thermal and nutritional stress and assessed the correlation between response of developmental time and body size. While we found significant genetic variation in development time plasticity, it was a poor predictor of body size among genotypes. Our results therefore suggest that multiple developmental pathways could generate genetic variation in body size plasticity. Our study emphasizes the need to better understand genetic variation in plasticity within a population, which will help determine the potential for populations to adapt to ongoing environmental change.     

Re-establishment of clinal variation in flowering time among introduced populations of purple loosestrife (Lythrum salicaria, Lythraceae)

Range expansion during biological invasion requires that invaders adapt to geographical variation in climate, which should yield latitudinal clines in reproductive phenology. We investigated geographic variation in life history among 25 introduced populations of Lythrum salicaria, a widespread European invader of North American wetlands. We detected a strong latitudinal cline in initiation of flowering and size at flowering, which paralleled that reported among native populations. Plants from higher latitudes flowered earlier and at a smaller size than those from lower latitudes, even when raised in a uniform glasshouse. Early flowering was associated with greatly reduced reproductive output, but this was not associated with latitudinal variation in abundance, and probably did not result from a genetic correlation between time to and size at flowering. As introduction to North America c. 200 years ago, L. salicaria has re-established latitudinal clines in life history, probably as an evolutionary response to climatic selection.     

The importance of listening: juvenile allocation shifts in response to acoustic cues of the social environment

The social environment has a strong effect on the strength and direction of sexual selection. Juveniles, however, often have social cues that signal the current competitive environment which may provide cues of future competitive challenges. Here we demonstrate that juvenile crickets (Teleogryllus commodus) use the calls of surrounding adult males as a cue of the quality and density of rivals/mates they are likely to encounter. We reared hatchling crickets in six acoustic environments that varied in the density and quality of calls and demonstrate that individuals modified their development rate, phenotype and behaviour at maturity. Males matured more rapidly at a smaller size and called more when reared in a low competition environment. In contrast, males delayed maturity to grow larger when faced with an increased density of high-quality males. Females matured more rapidly when reared in a high density of high-quality males and allocated proportionately more resources towards egg production. A second experiment limiting nutrient availability demonstrates sex-specific allocation shifts in the last stadium when cues are most reliable. Our results demonstrate that the social environment significantly affects allocation strategies and phenotypes, highlighting the importance of juvenile experience and competitive context when examining fitness and selection.     

Trait variation in response to varying winter temperatures,diversity patterns and signatures of selection along the latitudinal distribution of the widespread grassland plant Arrhenatherum elatius

Across Europe, genetic diversity can be expected to decline toward the North because of stochastic and selective effects which may imply diminished phenotypic variation and less potential for future genetic adaptations to environmental change. Understanding such latitudinal patterns can aid provenance selection for breeding or assisted migration approaches. In an experiment simulating different winter temperatures, we assessed quantitative trait variation, genetic diversity, and differentiation for natural populations of the grass Arrhenatherum elatius originating from a large latitudinal gradient. In general, populations from the North grew smaller and had a lower flowering probability. Toward the North, the absolute plastic response to the different winter conditions as well as heritability for biomass production significantly declined. Genetic differentiation in plant height and probability of flowering were very strong and significantly higher than under neutral expectations derived from SNP data, suggesting adaptive differentiation. Differentiation in biomass production did not exceed but mirrored patterns for neutral genetic differentiation, suggesting that migration‐related processes caused the observed clinal trait variation. Our results demonstrate that genetic diversity and trait differentiation patterns for A. elatius along a latitudinal gradient are likely shaped by both local selection and genetic drift.     

Evolution and plasticity of anuran larval development in response to desiccation. A comparative analysis

Anurans breed in a variety of aquatic habitats with contrasting levels of desiccation risk, which may result in selection for faster development during larval stages. Previous studies suggest that species in ephemeral ponds reduce their developmental times to minimize desiccation risks, although it is not clear how variation in desiccation risk affects developmental strategies in different species. Employing a comparative phylogenetic approach including data from published and unpublished studies encompassing 62 observations across 30 species, we tested if species breeding in ephemeral ponds (High risk) develop faster than those from permanent ponds (Low risk) and/or show increased developmental plasticity in response to drying conditions. Our analyses support shorter developmental times in High risk, primarily by decreasing body mass at metamorphosis. Plasticity in developmental times was small and did not differ between groups. However, accelerated development in High risk species generally resulted in reduced sizes at metamorphosis, while some Low risk species were able compensate this effect by increasing mean growth rates. Taken together, our results suggest that plastic responses in species breeding in ephemeral ponds are constrained by a general trade-off between development and growth rates.     

Developmental inflexibility of larval tapeworms in response to resource variation

The timing of habitat switching in organisms with complex life cycles is an important life history characteristic that is often influenced by the larval growth environment. Under starvation, longer developmental times are frequently observed, probably as a consequence of developmental thresholds, but prolonged ontogeny sometimes also occurs under good conditions, as organisms may take advantage of the large potential gains in body size. I investigated whether variation in growth conditions affects the larval development time of a complex life cycle tapeworm (Schistocephalus solidus) in its copepod first host. Moreover, I reviewed patterns of developmental plasticity in larval tapeworms to assess the generality of my findings. Copepod starvation weakly retarded parasite growth but did not affect development. Worms grew bigger in larger copepods, but they developed at a similar rate in large and small hosts. Thus, S. solidus does not delay ontogeny under good conditions nor does it fail to reach a developmental threshold under poor conditions. Although unusual in comparison to free-living organisms, such inflexibility is common in tapeworms. Plasticity, namely prolonged ontogeny, has been mainly observed at high infection intensities. For S. solidus, there were large cross-environment genetic correlations for development, suggesting there may be genetic constraints on the evolution of developmental plasticity.     

Global biogeography of mating system variation in seed plants

Latitudinal gradients in biotic interactions have been suggested as causes of global patterns of biodiversity and phenotypic variation. Plant biologists have long speculated that outcrossing mating systems are more common at low than high latitudes owing to a greater predictability of plant–pollinator interactions in the tropics; however, these ideas have not previously been tested. Here, we present the first global biogeographic analysis of plant mating systems based on 624 published studies from 492 taxa. We found a weak decline in outcrossing rate towards higher latitudes and among some biomes, but no biogeographic patterns in the frequency of self‐incompatibility. Incorporating life history and growth form into biogeographic analyses reduced or eliminated the importance of latitude and biome in predicting outcrossing or self‐incompatibility. Our results suggest that biogeographic patterns in mating system are more likely a reflection of the frequency of life forms across latitudes rather than the strength of plant–pollinator interactions.     

Evolution in stressful environments II: adaptive value and costs of plasticity in response to low light in Sinapis arvensis

Plants possess a remarkable capacity to alter their phenotype in response to the highly heterogeneous light conditions they commonly encounter in natural environments. In the present study with the weedy annual plant Sinapis arvensis, we (a) tested for the adaptive value of phenotypic plasticity in morphological and life history traits in response to low light and (b) explored possible fitness costs of plasticity. Replicates of 31 half-sib families were grown individually in the greenhouse under full light and under low light (40% of ambient) imposed by neutral shade cloth. Low light resulted in a large increase in hypocotyl length and specific leaf area (SLA), a reduction in juvenile biomass and a delayed onset of flowering. Phenotypic selection analysis within each light environment revealed that selection favoured large SLA under low light, but not under high light, suggesting that the observed increase in SLA was adaptive. In contrast, plasticity in the other traits measured was maladaptive (i.e. in the opposite direction to that favoured by selection in the low light environment). We detected significant additive genetic variance in plasticity in most phenotypic traits and in fitness (number of seeds). Using genotypic selection gradient analysis, we found that families with high plasticity in SLA had a lower fitness than families with low plasticity, when the effect of SLA on fitness was statistically kept constant. This indicates that plasticity in SLA incurred a direct fitness cost. However, a cost of plasticity was only expressed under low light, but not under high light. Thus, models on the evolution of phenotypic plasticity will need to incorporate plasticity costs that vary in magnitude depending on environmental conditions.     

Sources of (co)variation in alternative siring routes available to male great tits (Parus major)

Males of socially monogamous species can increase their siring success via within‐pair and extra‐pair fertilizations. In this study, we focused on the different sources of (co)variation between these siring routes, and asked how each contributes to total siring success. We quantified the fertilization routes to siring success, as well as behaviors that have been hypothesized to affect siring success, over a five‐year period for a wild population of great tits Parus major. We considered siring success and its fertilization routes as “interactive phenotypes” arising from phenotypic contributions of both members of the social pair. We show that siring success is strongly affected by the fecundity of the social (female) partner. We also demonstrate that a strong positive correlation between extra‐pair fertilization success and paternity loss likely constrains the evolution of these two routes. Moreover, we show that more explorative and aggressive males had less extra‐pair fertilizations, whereas more explorative females laid larger clutches. This study thus demonstrates that (co)variation in siring routes is caused by multiple factors not necessarily related to characteristics of males. We thereby highlight the importance of acknowledging the multilevel structure of male fertilization routes when studying the evolution of male mating strategies.     

Offspring growth and mobility in response to variation in parental care: a comparison between populations

Life history theory emphasizes the importance of trade‐offs in how time and energy are allocated to the competing demands of growth, fecundity, and survival. However, avian studies have historically emphasized the importance of resource acquisition over resource allocation to explain geographic variation in fecundity, parental care, and offspring development. We compared the brood sizes and nestling mass and feather growth trajectories between orange‐crowned warblers Oreothlypis celata breeding in Alaska versus California, and used 24‐h video recordings to study the relationship between parental care and growth rates. Per‐offspring provisioning rates were highest in the smallest broods, and food delivery was positively correlated with nestling growth over the 24‐h period only in Alaska. Females in Alaska spent more time brooding, and juveniles there showed faster feather growth and earlier mobility compared with those in California. We also found differences in the energetic and nutritional content of insect larvae that could facilitate the observed differences in nestling growth relative to food provisioning. Our results point to the potential importance of food quality and parental provisioning of warmth, in addition to food, for explaining avian growth patterns. We highlight the need to quantify multiple dimensions of parental care and of offspring growth and development, and to better understand the relationships between feather growth, nestling period length, and fledgling mobility.     

When to cut your losses: Dispersal allocation in an asexual filamentous fungus in response to competition

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Eco‐evolutionary dynamics in response to selection on life‐history

Understanding the consequences of environmental change on ecological and evolutionary dynamics is inherently problematic because of the complex interplay between them. Using invertebrates in microcosms, we characterise phenotypic, population and evolutionary dynamics before, during and after exposure to a novel environment and harvesting over 20 generations. We demonstrate an evolved change in life‐history traits (the age‐ and size‐at‐maturity, and survival to maturity) in response to selection caused by environmental change (wild to laboratory) and to harvesting (juvenile or adult). Life‐history evolution, which drives changes in population growth rate and thus population dynamics, includes an increase in age‐to‐maturity of 76% (from 12.5 to 22 days) in the unharvested populations as they adapt to the new environment. Evolutionary responses to harvesting are outweighed by the response to environmental change (~ 1.4 vs. 4% change in age‐at‐maturity per generation). The adaptive response to environmental change converts a negative population growth trajectory into a positive one: an example of evolutionary rescue.     

Growth rate adjustment of two Drosophila parasitoids in response to the developmental stage of hosts

1. Generalist koinobiont parasitoids often exhibit high flexibility in their development; their larvae shorten or prolong the developmental period depending on the host quality at parasitisation. However, flexibility of the growth rate of parasitoid larvae has rarely been investigated so far. 2. This study investigated how the koinobiont parasitoid wasps Asobara japonica and Leptopilina ryukyuensis regulate their larval growth when they parasitise host Drosophila larvae with varying larval periods. 3. In both parasitoid species, the preimaginal period was longer when they parasitised 1‐day‐old larvae of Drosophila rufa than when they parasitised older larvae of D. rufa or when they parasitised larvae of Drosophila simulans, a species with a shorter larval period than D. rufa. After host pupariation, A. japonica accelerated its growth, thereby showing a biphasic growth curve. On the other hand, L. ryukyuensis did not accelerate its growth after host pupariation. 4. Growth retardation of parasitoid larvae in 1‐day‐old D. rufa larvae would contribute to avoiding excess growth before host pupariation, because the excess growth of parasitoid larvae would have negative effects on host growth. The growth rate acceleration of A. japonica after host pupariation suggests that they enhance resource utilisation in a host that has reached maximum body mass. It remains uncertain as to why L. ryukuensis does not show clear accelerated growth after host pupariation. Nonetheless, these results suggest that parasitoid larvae have the ability to detect the developmental stage of hosts in a species‐specific manner.