Early and late developmental arrest as complementary embryonic bet‐hedging strategies in African killifish

The production of dormant eggs is a crucial adaptation for African killifish of the genus Nothobranchius to survive in temporary waters. These habitats are often characterized by unpredictable variation in the suitability of growing seasons as a result of variable lengths of inundations and temporary colonization by piscivorous fish. Incomplete hatching could enable killifish to buffer against reproductive failure during unsuitable inundations. Although this phenomenon has been tentatively linked to variation in dormancy states, it has never been investigated under controlled conditions and its viability as a bet hedging strategy to distribute offspring over several inundations remains unclear. In the present study, we used common garden experiments to assess the contribution of environmental modulation and bet hedging to delayed hatching in Nothobranchius killifish by testing the feasibility of arrested development in the presence and absence of environmental cues. Overall, the results confirmed that the presence of cues signalling a threat (predator kairomones) inhibited hatching. However, delayed development also occurred independent of cues and was regulated at two stages. Developmental arrest in energy‐efficient dormancy stages could present a means for long‐term bet hedging over years, whereas arrest in the energy‐consuming final stage may serve a similar purpose over shorter time scales. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 941–948.     

Local adaptation and embryonic plasticity affect antipredator traits in hatchling pond snails

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Risk‐induced hatching timing shows low heritability and evolves independently of spontaneous hatching in red‐eyed treefrogs

Plasticity in the timing of transitions between stages of complex life cycles allows organisms to adjust their growth and development to local environmental conditions. Genetic variation in such plasticity is common, but the evolution of context‐dependent transition timing may be constrained by information reliability, lag‐time and developmental constraints. We studied the genetic architecture of hatching plasticity in embryos of the red‐eyed treefrog (Agalychnis callidryas) in response to simulated predator attacks using a series of paternal and maternal half‐sibs from a captive breeding colony of wild‐collected animals. We compared the developmental timing of induced early hatching across sibships and estimated cross‐environment genetic correlations between induced and spontaneous hatching traits. Additive genetic variance for induced early hatching was very low, indicating a constraint on the short‐term evolution of earlier hatching timing. This constraint is likely related to the maturation of the hatching mechanism. The most plastic genotypes produced the most extreme spontaneous hatching phenotypes, indicating that developmental range, per se, is not constrained. Cross‐environment genetic correlation in hatching timing was negligible, so the evolution of spontaneous hatching in this species has not depended on the evolution of risk‐induced hatching and vice versa.     

Predation on freshwater snails in Miocene Lake Steinheim: a trigger for intralacustrine evolution?

Shells of the freshwater gastropods Gyraulus trochiformis (Planorbidae or ramshorn snails) and Bania pseudoglobula (formerly Pseudamnicola, Hydrobiidae) from Miocene Steinheim Basin in SW Germany contain small holes with a mean diameter of 0.8 mm. Analyses of comparable holes are so far unknown from fossil or extant assemblages of freshwater shells. This analysis of the perforated shells suggests that the holes were not formed by post‐depositional or pure taphonomic processes. Instead, they were most likely produced by predators. This analysis widens the means for identification of predation on freshwater snail shells that can be used in other palaeolimnological studies. The co‐occurrence of fish teeth and perforated shells in the studied samples as well as the perforation features suggest that the predator was either barbel or tench fish. The correlation between shell sizes and hole diameters suggests a size relationship between predator and prey that may generally be related to gape‐limited fish predators. The co‐occurrence of perforated shells in these lake sediments with a dominance of large and armoured shells suggest that these larger shells with protuberances and knobs could not be crushed by the gape‐limited fish predators. This analysis is the basis for a hypothesis that the endemic evolution of Gyraulus in Lake Steinheim, with some varied forms of shell thickness and morphology, was triggered by a predator–prey relationship based on adaptations to avoid shell‐breaking predators.     

Predation risk affects egg mortality and carry over effects in the larval stages in damselflies

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REDUCTION OF THE PECTORAL SPINE AND GIRDLE IN DOMESTICATED CHANNEL CATFISH IS LIKELY CAUSED BY CHANGES IN SELECTION PRESSURE

Locked pectoral spines of the Channel Catfish Ictalurus punctatus more than double the fish's width and complicate ingestion by gape‐limited predators. The spine mates with the pectoral girdle, a robust structure that anchors the spine. This study demonstrates that both spine and girdle exhibit negative allometric growth and that pectoral spines and girdles are lighter in domesticated than in wild Channel Catfish. This finding could be explained by changes in selection pressure for spine growth during domestication or by an epigenetic effect in which exposure to predators in wild fish stimulates pectoral growth. We tested the epigenetic hypothesis by exposing domesticated Channel Catfish fingerlings to Largemouth Bass Micropterus salmoides predators for 13 weeks. Spines and girdles grow isometrically in the fingerlings, and regression analysis indicates no difference in proportional pectoral growth between control and predator‐exposed fish. Therefore a change in selection pressure likely accounts for smaller pectoral growth in domesticated Channel Catfish. Decreasing spine growth in older fish suggests anti‐predator functions are most important in smaller fish. Additionally, growth of the appendicular and axial skeleton is controlled differentially, and mechanical properties of the spine and not just its length are an important component of this defensive adaptation.     

Metazoan parasites of African annual killifish (Nothobranchiidae): abundance,diversity, and their environmental correlates

Estimates of biodiversity and its global patterns are affected by parasite richness and specificity. Despite this, parasite communities are largely neglected in biodiversity estimates, especially in the tropics. We studied the parasites of annual killifish of the genus Nothobranchius that inhabit annually desiccating pools across the African savannah and survive the dry period as developmentally arrested embryos. Their discontinuous, non‐overlapping generations make them a unique organism in which to study natural parasite fauna. We investigated the relationship between global (climate and altitude) and local (pool size, vegetation, host density and diversity, and diversity of potential intermediate hosts) environmental factors and the community structure of killifish parasites. We examined metazoan parasites from 21 populations of four host species (Nothobranchius orthonotus, N. furzeri, N. kadleci, and N. pienaari) across a gradient of aridity in Mozambique. Seventeen parasite taxa were recorded, with trematode larval stages (metacercariae) being the most abundant taxa. The parasites recorded were both allogenic (life cycle includes non‐aquatic host; predominantly trematodes) and autogenic (cycling only in aquatic hosts; nematodes). The parasite abundance was highest in climatic regions with intermediate aridity, while parasite diversity was associated with local environmental characteristics and positively correlated with fish species diversity and the amount of aquatic vegetation. Our results suggest that parasite communities of sympatric Nothobranchius species are similar and dominated by the larval stages of generalist parasites. Therefore, Nothobranchius serve as important intermediate or paratenic hosts of parasites, with piscivorous birds and predatory fish being their most likely definitive hosts.     

Feedback between size balance and consumption strongly affects the consequences of hatching phenology in size‐dependent predator–prey interactions

In many size‐dependent predator–prey systems, hatching phenology strongly affects predator–prey interaction outcomes. Early‐hatched predators can easily consume prey when they first interact because they encounter smaller prey. However, this process by itself may be insufficient to explain all predator–prey interaction outcomes over the whole interaction period because the predator–prey size balance changes dynamically throughout their ontogeny. We hypothesized that hatching phenology influences predator–prey interactions via a feedback mechanism between the predator–prey size balance and prey consumption by predators. We experimentally tested this hypothesis in an amphibian predator–prey model system. Frog tadpoles Rana pirica were exposed to a predatory salamander larva Hynobius retardatus that had hatched 5, 12, 19 or 26 days after the frog tadpoles hatched. We investigated how the salamander hatch timing affected the dynamics of prey mortality, size changes of both predator and prey, and their subsequent life history (larval period and size at metamorphosis). The predator–prey size balance favoured earlier hatched salamanders, which just after hatching could successfully consume more frog tadpoles than later hatched salamanders. The early‐hatched salamanders grew rapidly and their accelerated growth enabled them to maintain the predator‐superior size balance; thus, they continued to exert strong predation pressure on the frog tadpoles in the subsequent period. Furthermore, frog tadpoles exposed to the early‐hatched salamanders were larger at metamorphosis and had a longer larval period than other frog tadpoles. These results suggest that feedback between the predator‐superior size balance and prey consumption is a critical mechanism that strongly affects the impacts of early hatching of predators in the short‐term population dynamics and life history of the prey. Because consumption of large nutrient‐rich prey items supports the growth of predators, a similar feedback mechanism may be common and have strong impacts on phenological shifts in size‐dependent trophic relationships.     

Evidence for genetic differentiation in timing of maturation among nine‐spined stickleback populations

Timing of maturation is an important life‐history trait that is likely to be subjected to strong natural selection. Although population differences in timing of maturation have been frequently reported in studies of wild animal populations, little is known about the genetic basis of this differentiation. Here, we investigated population and sex differences in timing of maturation within and between two nine‐spined stickleback (Pungitius pungitius) populations in a laboratory breeding experiment. We found that fish from the high‐predation marine population matured earlier than fish from the low‐predation pond population and males matured earlier than females. Timing of maturation in both reciprocal hybrid crosses between the two populations was similar to that in the marine population, suggesting that early timing of maturation is a dominant trait, whereas delayed timing of maturation in the pond is a recessive trait. Thus, the observed population divergence is suggestive of strong natural selection against early maturation in the piscine‐predator‐free pond population.     

Feeding preferences of an invasive Ponto‐Caspian goby for native and non‐native gammarid prey

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Effects of predation environment and food availability on somatic growth in the Livebearing Fish Brachyrhaphis rhabdophora (Pisces: Poeciliidae)

Variation in somatic growth rates is of great interest to biologists because of the relationship between growth and other fitness‐determining traits, and it results from both genetic and environmentally induced variation (i.e. plasticity). Theoretical predictions suggest that mean somatic growth rates and the shape of the reaction norm for growth can be influenced by variation in predator‐induced mortality rates. Few studies have focused on variation in reaction norms for growth in response to resource availability between high‐predation and low‐predation environments. We used juvenile Brachyrhaphis rhabdophora from high‐predation and low‐predation environments to test for variation in mean growth rates and for variation in reaction norms for growth at two levels of food availability in a common‐environment experiment. To test for variation in growth rates in the field, we compared somatic growth rates in juveniles in high‐predation and low‐predation environments. In the common‐environment experiment, mean growth rates did not differ between fish from differing predation environments, but the interaction between predation environment and food level took the form of a crossing reaction norm for both growth in length and mass. Fish from low‐predation environments exhibited no significant difference in growth rate between high and low food treatments. In contrast, fish from high‐predation environments exhibited variation in growth rates between high and low food treatments, with higher food availability resulting in higher growth rates. In the field, individuals in the high‐predation environment grow at a faster rate than those in low‐predation environments at the smallest sizes (comparable to sizes in the common‐environment experiment). These data provide no evidence for evolved differences in mean growth rates between predation environments. However, fish from high‐predation environments exhibited greater plasticity in growth rates in response to resource availability suggesting that predation environments may exhibit increased variation in food availability for prey fish and consequent selection for plasticity.     

Squeezing out the last egg—annual fish increase reproductive efforts in response to a predation threat

Both constitutive and inducible antipredator strategies are ubiquitous in nature and serve to maximize fitness under a predation threat. Inducible strategies may be favored over constitutive defenses depending on their relative cost and benefit and temporal variability in predator presence. In African temporary ponds, annual killifish of the genus Nothobranchius are variably exposed to predators, depending on whether larger fish invade their habitat from nearby rivers during floods. Nonetheless, potential plastic responses to predation risk are poorly known. Here, we studied whether Nothobranchius furzeri individuals adjust their life history in response to a predation threat. For this, we monitored key life history traits in response to cues that signal the presence of predatory pumpkinseed sunfish (Lepomis gibbosus). While growth rate, adult body size, age at maturation, and initial fecundity were not affected, peak and total fecundity were higher in the predation risk treatment. This contrasts with known life history strategies of killifish from permanent waters, which tend to reduce reproduction in the presence of predators. Although our results show that N. furzeri individuals are able to detect predators and respond to their presence by modulating their reproductive output, these responses only become evident after a few clutches have been deposited. Overall our findings suggest that, in the presence of a predation risk, it can be beneficial to increase the production of life stages that can persist until the predation risk has faded.     

Temporal variation in behavioral responses to dietary cues from a gape‐limited predator in tadpole prey: A test of the phylogenetic relatedness hypothesis

The ability of prey to recognize and adequately respond to predators determines their survival. Predator‐borne, post‐digestion dietary cues represent essential information for prey about the identity and the level of risk posed by predators. The phylogenetic relatedness hypothesis posits that prey should respond strongly to dietary cues from closely related heterospecifics but respond weakly to such cues from distantly related prey, following a hierarchical pattern. While such responses have mostly been observed in prey at their first encounter with predators, whether prey maintain such hierarchical levels of investment through time remains unclear. We investigated this question by exposing Rhacophorus arboreus tadpoles to the non‐consumptive effect of gape‐limited newt predators Cynops pyrrhogaster that were fed one of five prey diets across a gradient of phylogenetic relatedness: frog tadpoles (Rhacophorus arboreus, Rhacophorus schlegelii, Pelophylax nigromaculatus, and Hyla japonica) and medaka fish (Oryzias latipes). Predators’ diet, time, and their interaction significantly influenced tadpole activity level. We found support for the phylogenetic relatedness hypothesis: Investments in defense were stronger to cues from tadpole diets than to cues from fish diet. However, such a hierarchical response was recorded only in the first four days following predator exposure, then gradually disappear by day 8 on which the tadpoles exhibited similar activity level across all predator treatments. The findings suggest that, at least under the threat of gape‐limited predators, prey use phylogenetic information to evaluate risk and appropriately invest in defense during early encounters with predators; however, energy requirements may prevent prey from maintaining a high level of defense over long exposure to predation risk.     

Predation environment affects boldness temperament of neotropical livebearers

Behavioral traits of individuals are important phenotypes that potentially interact with many other traits, an understanding of which may illuminate the evolutionary forces affecting populations and species. Among the five axes of temperament is the propensity to behave boldly in the presence of a perceived risk. To determine the effect of different predatorial regimes on boldness and fearfulness, we assessed the behavior of individuals in a novel portable swim chamber (i.e., forced open‐field test) by Brachyrhaphis rhabdophora (n = 633). We used an information theoretic framework to compare generalized (logistic) linear fixed‐effects models of predatorial regime (predator‐free [n = 6] and predator [n = 4] sites), sex, and standard length (SL). Fish from predator sites were much more fearful in the novel arena than fish from nonpredator sites. This varied by length, but not by sex. At 48 mm SL, fish from nonpredator sites were 4.9 times more likely to express bold behavior (ambulation) in the novel swim chamber as fish from predator sites. Probabilities of “ambulating” within the swim chamber increased with size for nonpredator sites and decreased with size for predator sites.     

Sex,growth rate,rank order after brood reduction,and hatching date affect first‐year survival of long‐lived Herring Gulls

Among most species of birds, survival from hatching throughout the first year of life is generally lower than subsequent survival rates. Survival of young birds during their first year may depend on a combination of selection, learning, unpredictable resources, and environmental events (i.e., post‐fledging factors). However, knowledge about post‐fledging development in long‐lived species is usually limited due to a lengthy immature stage when individuals are generally unobservable. Therefore, pre‐fledging characteristics are often used to predict the survival of young birds. We assessed effects of nestling growth rates, hatching date, hatching asynchrony, brood size and rank order after brood reduction, and sex on first‐year survival of 137 fledglings using a mark‐resighting analysis. We found that the survival probability (Φ_1yr = 0.39) of first‐year Herring Gulls (Larus argentatus) in our study colony located at the outer port of Zeebrugge (Belgium) was lower than that of older individuals (Φ_>1yr = 0.75). All 10 models best supported by our data included nestling growth rate, suggesting that variability in first‐year survival may be linked primarily to individual variation in growth. First‐year survival was negatively correlated with hatching date and rank order after brood reduction. Hence, carry‐over effects of breeding season events such as timing of breeding, early development, and social status had an influence on survival of Herring Gulls after fledging. Furthermore, we found sex‐biased mortality in first‐year Herring Gulls, with females (Φ_1yr = 0.45) surviving better than males (Φ_1yr = 0.38). Although adult survival is generally regarded as the key parameter driving population trajectories in long‐lived species, juvenile survival has recently been acknowledged as an important source of variability in population growth rates. Thus, increasing our knowledge of factors affecting age‐specific survival rates is necessary to improve our understanding of population dynamics and ultimately life‐history variation.     

Feeding habits and predator‐prey size relationships of mandarin fish Siniperca chuatsi (Basilewsky) in a shallow lake,central China

The diet and predator‐prey size relationships of mandarin fish Siniperca chuatsi (Basilewsky) in Lake Xiaosihai along the middle reach of the Yangtze River were studied through stomach content analysis. A total of 401 specimens (91–539 mm total length) were collected in 2007. The diet was dominated by topmouth gudgeon Pseudorasbora parva, sharpbelly Hemiculter leucisculus, redfin culter Cultrichthys erythropterus, and crucian carp Carassius auratus, with significant seasonal and ontogenetic differences. Ontogenetic variation in diet was apparent that larger prey items such as crucian carp and redfin culter became more common, while smaller prey such as topmouth gudgeon, bitterlings and shrimps gradually declined in the larger fish. Mandarin fish total length (TL) was strongly related to mouth gape width (GW) and gape height (GH). Mandarin fish TL and prey fish TL as well as mandarin fish GW and prey fish body depth (BD) were positively and linearly related for sharpbelly, redfin culter and crucian carp. Strong size selectivity for topmouth gudgeon, sharpbelly and redfin culter as prey indicated that the piscivorous mandarin fish can have potential impact on the population size structure of the three prey fish.     

Alternative intrapopulation life‐history strategies and their trade‐offs in an African annual fish

In ephemeral habitats, the same genotypes cope with unpredictable environmental conditions, favouring the evolution of developmental plasticity and alternative life‐history strategies (ALHS). We tested the existence of intrapopulation ALHS in an annual killifish, Nothobranchius furzeri, inhabiting temporary pools. The pools are either primary (persisting throughout the whole rainy season) or secondary (refilled after desiccation of the initial pool), representing alternative niches. The unpredictable conditions led to the evolution of reproductive bet‐hedging with asynchronous embryonic development. We used a common garden experiment to test whether the duration of embryonic period is associated with post‐embryonic life‐history traits. Fish with rapid embryonic development (secondary pool strategy, high risk of desiccation) produced phenotypes with more rapid life‐history traits than fish with slow embryonic development (primary pool strategy). The fast fish were smaller at hatching but had larger yolk sac reserves. Their post‐hatching growth was more rapid, and they matured earlier. Further, fast fish grew to a smaller body size and died earlier than slow fish. No differences in fecundity, propensity to mate or physiological ageing were found, demonstrating a combination of plastic responses and constraints. Such developmentally related within‐population plasticity in life history is exceptional among vertebrates.     

A wide window of migration phenology captures inter‐annual variability of favourable conditions: Results of a whole‐lake experiment with juvenile Pacific salmon

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GAPE‐LIMITED PREDATORS AS AGENTS OF SELECTION ON THE DEFENSIVE MORPHOLOGY OF AN INVASIVE INVERTEBRATE

Invasive species have widespread and pronounced effects on ecosystems and adaptive evolution of invaders is often considered responsible for their success. Despite the potential importance of adaptation to invasion, we still have limited knowledge of the agents of natural selection on invasive species. Bythotrephes longimanus, a cladoceran zooplankton, invaded multiple Canadian Shield lakes over the past several decades. Bythotrephes have a conspicuous caudal process (tail spine) that provides a morphological defense against fish predation. We measured viability selection on the longest component of the Bythotrephes spine, the distal spine segment, through a comparison of the lengths of first and second instar Bythotrephes collected from lakes differing in the dominance of gape‐limited predation (GLP) and nongape‐limited predation (NGLP) by fish. We found that natural selection varied by predator gape‐limitation, with strong selection (selection intensity: 0.20–0.79) for increased distal spine length in lakes dominated by GLP, and no significant selection in lakes dominated by NGLP. Further, distal spine length was 17% longer in lakes dominated by GLP, suggesting the possibility of local adaptation. As all study lakes were invaded less than 20 years prior to our collections, our results suggest rapid divergence in defensive morphology in response to selection from fish predators.     

Experimental evolution of bet hedging in rotifer diapause traits as a response to environmental unpredictability

The adaptive response of organisms to unpredictable environments is increasingly recognized as a central topic in fundamental and applied evolutionary ecology. Selection due to environmental unpredictability can act on multiple traits of an organism's life cycle to reduce the impact of high environmental variance. The aim of this research was to study how unpredictability selects for diapause traits: 1) the timing of sex (a proxy of the timing of diapausing egg production), and 2) the diapausing egg hatching fraction (a proxy of diapause duration). We used an experimental evolution approach with the facultative sexual rotifer Brachionus plicatilis. Laboratory populations experiencing two contrasting regimes of environmental fluctuation (predictable versus unpredictable) evolved divergently over a short time span (< 77 days). The populations under the unpredictable regime showed an earlier initiation of sexual reproduction and a lower hatching fraction of diapausing eggs than populations under the predictable regime. These findings demonstrate empirically the existence of bet‐hedging strategies in B. plicatilis regarding both traits, consistent with theoretical predictions of bet‐hedging evolution under conditions of unpredictable environmental variance. Given that scenarios of increased environmental variability are expected to occur in the near future, a comprehensive understanding of the role of bet‐hedging strategies is necessary for predicting population responses to environmental change.