Why we cannot always expect life history strategies to directly inform on sensitivity to environmental change.

Variation in life history traits in animals and plants can often be structured along major axes of life history strategies. The position of a species along these axes can inform on their sensitivity to environmental change. For example, species with slow life histories are found to be less sensitive in their long-term population responses to environmental change than species with fast life histories. This provides a tantalizing link between sets of traits and population responses to change, contained in a highly generalizable theoretical framework. Life history strategies are assumed to reflect the outcome of life history tradeoffs that, by their very nature, act at the individual level. Examples include the tradeoff between current and future reproductive success, and allocating energy into growth versus reproduction. But the importance of such tradeoffs in structuring population-level responses to environmental change remains understudied. We aim to increase our understanding of the link between individual-level life history tradeoffs and the structuring of life history strategies across species, as well as the underlying links to population responses to environmental change. We find that the classical association between lifehistory strategies and population responses to environmental change breaks down when accounting for individual-level tradeoffs and energy allocation. Therefore, projecting population responses to environmental change should not be inferred based only on a limited set of species traits. We summarize our perspective and a way forward in a conceptual framework.

Spatial and temporal analysis of juvenile blacktip reef shark (Carcharhinus melanopterus) demographies identifies critical habitats.

Reef shark species have undergone sharp declines in recent decades, as they inhabit coastal areas, making them an easy target in fisheries (i.e., sharks are exploited globally for their fins, meat, and liver oil) and exposing them to other threats (e.g., being part of by-catch, pollution, and climate change). Reef sharks play a critical role in coral reef ecosystems, where they control populations of smaller predators and herbivorous fishes either directly via predation or indirectly via behavior, thus protecting biodiversity and preventing potential overgrazing of corals. The urgent need to conserve reef shark populations necessitates a multifaceted approach to policy at local, federal, and global levels. However, monitoring programmes to evaluate the efficiency of such policies are lacking due to the difficulty in repeatedly sampling free-ranging, wild shark populations. Over nine consecutive years, we monitored juveniles of the blacktip reef shark (Carcharhinus melanopterus) population around Moorea, French Polynesia, and within the largest shark sanctuary globally, to date. We investigated the roles of spatial (i.e., sampling sites) and temporal variables (i.e., sampling year, season, and month), water temperature, and interspecific competition on shark density across 10 coastal nursery areas. Juvenile C. melanopterus density was found to be stable over 9 years, which may highlight the effectiveness of local and likely federal policies. Two of the 10 nursery areas exhibited higher juvenile shark densities over time, which may have been related to changes in female reproductive behavior or changes in habitat type and resources. Water temperatures did not affect juvenile shark density over time as extreme temperatures proven lethal (i.e., 33°C) in juvenile C. melanopterus might have been tempered by daily variation. The proven efficiency of time-series datasets for reef sharks to identify critical habitats (having the highest juvenile shark densities over time) should be extended to other populations to significantly contribute to the conservation of reef shark species.

Costs of weaponry: Unarmed males sire more offspring than armed males in a male-dimorphic mite.

Morphological structures used as weapons in male-male competition are not only costly to develop but are also probably costly to maintain during adulthood. Therefore, having weapons could reduce the energy available for other fitness-enhancing actions, such as post-copulatory investment. We tested the hypothesis that armed males make lower post-copulatory investments than unarmed males, and that this difference will be most pronounced under food-limited conditions. We performed two experiments using the male-dimorphic bulb mite Rhizoglyphus robini, in which males are either armed "fighters" or unarmed "scramblers." Firstly, we tested whether fighters and scramblers differed in their reproductive output after being starved or fed for 1 or 2 weeks. Secondly, we measured the reproductive output of scramblers and fighters (starved or fed) after one, two or three consecutive matings. Scramblers sired more offspring than fighters after 1 week, but scramblers and fighters only sired a few offspring after 2 weeks. Scramblers also sired more offspring than fighters at the first mating, and males rarely sired offspring after consecutive matings. Contrary to our hypothesis, the fecundity of starved and fed males did not differ. The higher reproductive output of scramblers suggests that, regardless of nutritional state, scramblers make larger post-copulatory investments than fighters. Alternatively, (cryptic) female choice generally favours scramblers. Why the morphs differed in their reproductive output is unclear. Neither morph performed well relatively late in life or after multiple matings. It remains to be investigated to what extent the apparent scrambler advantage contributes to the maintenance and evolution of male morph expression.

An eco-evolutionary feedback loop between population dynamics and fighter expression affects the evolution of alternative reproductive tactics.

Surprisingly, little is known about how eco-evolutionary feedback loops affect trait dynamics within a single population. Polymorphisms of discrete alternative phenotypes present ideal test beds to investigate this, as the alternative phenotypes typically exhibit contrasting demographic rates mediated through frequency or density dependence, and are thus differentially affected by selection. Alternative reproductive tactics (ARTs), like male fighters and sneakers, are an extreme form of discrete phenotype expression and occur across many taxa. Fighters possess weapons for male-male competition over access to mates, whereas sneakers are defenceless but adopt tactics like female-mimicking. Because fighters in some species mortally injure conspecifics, this raises the question whether fighter expression can feed back to affect population size and structure, thereby altering the selection gradient and evolutionary dynamics of ART expression in an eco-evolutionary feedback loop. Here, we investigated how the eco-evolutionary feedback loop between fighter expression and population size and structure affects the evolution and maintenance of ARTs. We introduced intraspecific killing by fighters in a two-sex, two-ART population model parameterized for the male dimorphic bulb mite (Rhizoglyphus robini) that includes life-history differences between the ARTs and a mating-probability matrix analogous to the classic hawk-dove game. Using adaptive dynamics, we found that the intraspecific killing by fighters can extend the range of life-history parameter values under which ARTs evolve, because fighters that kill other fighters decrease fighter fitness. This effect can be nullified when benefits from killing are incorporated, like increased reproduction through increased energy uptake. The eco-evolutionary feedback effects found here for a dimorphic trait likely also occur in other fitness-related traits, such as behavioural syndromes, parental care and niche construction traits. Current theoretical advances to model eco-evolutionary processes, and empirical steps towards unravelling the underlying drivers, pave the way for understanding how selection affects trait evolution in an eco-evolutionary feedback loop.

Trait-based predictions and responses from laboratory mite populations to harvesting in stochastic environments.

Predictions on population responses to perturbations are often derived from trait-based approaches like integral projection models (IPMs), but are rarely tested. IPMs are constructed from functions that describe survival, growth and reproduction in relation to the traits of individuals and their environment. Although these functions comprise biologically non-informative statistical coefficients within standard IPMs, model parameters of the recently developed dynamic energy budget IPM (DEB-IPM) are life-history traits like "length at maturation" and "maximum reproduction rate". Testing predictions from mechanistic IPMs against empirical observations can therefore provide functional insights into the links between individual life history, the environment and population dynamics. Here, we compared the population dynamics of the bulb mite (Rhizoglyphus robini) predicted by a DEB-IPM with those observed in an experiment where populations experienced daily food rations that were either positively correlated over time (red noise), negatively (blue noise) or uncorrelated (white noise). We also selectively harvested large adults in half of these populations. The model failed to generate detailed predictions of population structure as juvenile numbers were overestimated; likely because juvenile-adult interference competition was underestimated. The model performed well at the population level as, for both harvested and unharvested populations, simulations matched the observed, long-term stochastic growth rate λs . We next generalised the model to investigate how stochastic change affects mite λs , which correlated well with the frequency f of experiencing periods of good environment, but, due to the relationship between f and noise colour ρ, did not correlate well with shifts in ρ. The sensitivity of λs to perturbations in life-history parameters depended on the type of stochastic change, as well as population growth. Our findings show that responses to differential mortality depend on individual life-history traits, environmental characteristics and population growth. As long-term climate change causes ever greater environmental fluctuations, trait-based approaches will be increasingly important in predicting population responses to change. We therefore conclude by illustrating what questions can be examined with mechanistic trait-based models like the DEB-IPM, the answers to which will advance our knowledge of the functional links between individual traits, the environment and population dynamics.

Life-history consequences of bidirectional selection for male morph in a male-dimorphic bulb mite.

Intralocus sexual conflict (IASC) arises when males and females have different trait optima. Some males pursue different alternative reproductive tactics (ARTs) with different trait optima, resulting in different strengths of IASC. Consequently, for instance daughter fitness is differentially affected by her sire's morph. We tested if-and which-other life-history traits correlatively change in bidirectional, artificial selection experiments for ARTs. We used the male-dimorphic bulb mite Rhizoglyphus robini, the males of which are high-fitness 'fighters' or low-fitness 'scramblers'. Twice in each of the five generations of selection, we assessed clutch composition (number of mites of the various life stages present) and size (total number of offspring). Furthermore, we tracked offspring from egg to adulthood in the first and final generation to detect differences between selection lines in the size and duration of stages, and in maturation time. We found that selection for male morph increased the frequency of that morph. Furthermore, compared to fighter lines, scrambler lines produced more females, which laid larger eggs (in the final generations), and maintained a higher egg-laying rate for longer. Otherwise, our results showed no consistent differences between the selection lines in clutch size and composition, life stage size or duration, or maturation time. Though we found few correlated life-history trait changes in response to selection on male morph, the differences in egg laying rate and egg size suggest that IASC between fighters is costlier to females than IASC with scramblers. We hypothesize that these differences in reproductive traits allow fighter-offspring to perform better in small, declining populations but scrambler-offspring to perform better in large, growing populations.

Unsuccessful dispersal affects life history characteristics of natal populations: The role of dispersal related variation in vital rates.

Individuals that disperse from one habitat to another has consequences for individual fitness, population dynamics and gene flow. The fitness benefits accrued in the new habitat are traded off against costs associated with dispersal. Most studies focus on costs at settlement and effects on settlement populations; the influence of dispersal to natal populations is assessed by monitoring change in numbers due to emigration. However, the extent to which natal populations are affected when individuals that invest in dispersal fail to disperse/emigrate is unclear. Here, we use an Integral Projection Model (IPM) to assess how developing into a disperser affects natal population structure and growth. We do so using the bulb mite (Rhizoglyphus robini) as a study system. Bulb mites, in unfavourable environments, develop into a dispersal (deutonymph) stage during ontogeny; these individuals are called dispersers with individuals not developing into this stage called non-dispersers. We varied disperser expression and parameterised IPMs to describe three simulations of successful and unsuccessful dispersal: (i) 'no dispersal' - dispersal stage is excluded and demographic data are from non-disperser individuals; (ii) 'false dispersal' - dispersal stage included and demographic data from non-disperser individuals are used; (iii) 'true dispersal' - dispersal stage included and demographic data are from individuals that go through the dispersal stage and from non-disperser individuals. We found that the type of dispersal simulation (no dispersal < false dispersal < true dispersal) and disperser expression increases generation time and reduces lifetime reproductive success and population growth rate. Our findings show that disperser individuals that fail to leave, can change the structure and growth of natal populations.

Life-history differences favor evolution of male dimorphism in competitive games.

Many species exhibit two discrete male morphs: fighters and sneakers. Fighters are large and possess weapons but may mature slowly. Sneakers are small and have no weapons but can sneak matings and may mature quickly to start mating earlier in life than fighters. However, how differences in competitive ability and life history interact to determine male morph coexistence has not yet been investigated within a single framework. Here we integrate demography and game theory into a two-sex population model to study the evolution of strategies that result in the coexistence of fighters and sneakers. We incorporate differences in maturation time between the morphs and use a mating-probability matrix analogous to the classic hawk-dove game. Using adaptive dynamics, we show that male dimorphism evolves more easily in our model than in classic game theory approaches. Our results also revealed an interaction between life-history differences and sneaker competitiveness, which shows that demography and competitive games should be treated as interlinked mechanisms to understand the evolution of male dimorphism. Applying our approach to empirical data on bulb mites (Rhizoglyphus robini), coho salmon (Oncorhynchus kisutch), and bullhorned dung beetles (Onthophagus taurus) indicates that observed occurrences of male dimorphism are in general agreement with model predictions.

Correlative changes in life-history variables in response to environmental change in a model organism.

Global change alters the environment, including increases in the frequency of (un)favorable events and shifts in environmental noise color. However, how these changes impact the dynamics of populations, and whether these can be predicted accurately has been largely unexamined. Here we combine recently developed population modeling approaches and theory in stochastic demography to explore how life history, morphology, and average fitness respond to changes in the frequency of favorable environmental conditions and in the color of environmental noise in a model organism (an acarid mite). We predict that different life-history variables respond correlatively to changes in the environment, and we identify different life-history variables, including lifetime reproductive success, as indicators of average fitness and life-history speed across stochastic environments. Depending on the shape of adult survival rate, generation time can be used as an indicator of the response of populations to stochastic change, as in the deterministic case. This work is a useful step toward understanding population dynamics in stochastic environments, including how stochastic change may shape the evolution of life histories.

Effects of variation in nutrition on male morph development in the bulb mite Rhizoglyphus robini.

In male dimorphic species, growth influences morph expression and thereby the reproductive success of males. However, how variation in nutritional conditions affects male morph development and whether males can compensate for lost growth is poorly known. Here, we performed an experiment where males of the bulb mite (Rhizoglyphus robini)-which are fighters, able to kill other mites, or benign scramblers-were offered high quality food during the larval stage, but food of high or low quality during the protonymph and tritonymph (=final) stage. When food quality was low during the latter two stages, males matured smaller, later and were more likely to be a scrambler than when food quality was high. We found no evidence for compensatory growth: when males had low quality food only during the protonymph stage, they matured at the same age, but grew at a slower rate and matured at a smaller size than males that had high quality food throughout ontogeny. Furthermore, males that experienced this transient period of low food quality were less likely to mature as a fighter. Interestingly, scrambler increase in body size during the protonymph and tritonymph stages was always lower than that of fighters. Given the strong link between adult size and fitness, combined with the different development times and life histories of the male morphs, the lack of ability to compensate for a transient period of food deprivation during ontogeny is likely to have consequences for the dynamics of bulb mite populations.

Does frequency-dependence determine male morph survival in the bulb mite Rhizoglyphus robini?

Alternative reproductive phenotypes (ARPs) represent discrete morphological variation within a single sex; as such ARPs are an excellent study system to investigate the maintenance of phenotypic variation. ARPs are traditionally modelled as a mixture of pure strategies or as a conditional strategy. Most male dimorphisms are controlled by a conditional strategy, where males develop into a particular phenotype as a result of their condition which allows them to reach a certain threshold. Individuals that are unable to reach the threshold of a conditional strategy are considered to 'make the best of a bad job'; however, these individuals can have their own fitness merits. Given these fitness merits, condition-dependent selection alone is not sufficient to maintain a conditionally determined male dimorphism and other mechanisms, most likely frequency-dependent selection, are required. We studied in an experiment, the male dimorphic bulb mite Rhizoglyphus robini-where males are fighters that can kill other males or benign scramblers-to assess the strength of frequency-dependent survival in a high and low-quality environment. We found that male survival was frequency-dependent in the high-quality environment but not the low-quality environment. In the high-quality environment the survival curves of the two morphs crossed but the direction of frequency-dependence was opposite to what theory predicts.

DEBBIES Dataset to study Life Histories across Ectotherms.

Demographic models are used to explore how life history traits structure life history strategies across species. This study presents the DEBBIES dataset that contains estimates of eight life history traits (length at birth, puberty and maximum length, maximum reproduction rate, fraction energy allocated to respiration versus reproduction, von Bertalanffy growth rate, mortality rates) for 185 ectotherm species. The dataset can be used to parameterise dynamic energy budget integral projection models (DEB-IPMs) to calculate key demographic quantities like population growth rate and demographic resilience, but also link to conservation status or biogeographical characteristics. Our technical validation shows a satisfactory agreement between observed and predicted longevity, generation time, age at maturity across all species. Compared to existing datasets, DEBBIES accommodates (i) easy cross-taxonomical comparisons, (ii) many data-deficient species, and (iii) population forecasts to novel conditions because DEB-IPMs include a mechanistic description of the trade-off between growth and reproduction. This dataset has the potential for biologists to unlock general predictions on ectotherm population responses from only a few key life history traits.

Integrating developmental plasticity into eco-evolutionary population dynamics.

There are increasing calls to incorporate developmental plasticity into the framework of eco-evolutionary dynamics. The current way is via genotype-specified reaction norms in which inheritance and phenotype expression are gene-based. I propose a developmental system perspective in which phenotypes are formed during individual development in a process comprising a complex set of interactions that involve genes, biochemistry, somatic state, and the (a)biotic environment, and where the developmental system is the unit of phenotype evolution. I explain how the two perspectives differ in assumptions and predictions, which can be contrasted using cue-and-response systems of anticipatory or mitigating developmental plasticity. This can lead to new ways of eco-evolutionary thinking, and deliver important explanations of how populations respond to environmental change through evolved developmental plasticity.

Nutrient-dependent allometric plasticity in a male-diphenic mite.

Male secondary sexual traits often scale allometrically with body size. These allometries can be variable within species and may shift depending on environmental conditions, such as food quality. Such allometric plasticity has been hypothesized to initiate local adaptation and evolutionary diversification of scaling relationships, but is under-recorded, and its eco-evolutionary effects are not well understood. Here, we tested for allometric plasticity in the bulb mite (Rhizoglyphus robini), in which large males tend to develop as armed adult fighters with thickened third legs, while small males become adult scramblers without thickened legs. We first examined the ontogenetic timing for size- and growth-dependent male morph determination, using experimentally amplified fluctuations in growth rate throughout juvenile development. Having established that somatic growth and body size determine male morph expression immediately before metamorphosis, we examined whether the relationship between adult male morph and size at metamorphosis shifts with food quality. We found that the threshold body size for male morph expression shifts toward lower values with deteriorating food quality, confirming food-dependent allometric plasticity. Such allometric plasticity may allow populations to track prevailing nutritional conditions, potentially facilitating rapid evolution of allometric scaling relationships.

Mating status affects female choice when females are signalers.

Sexual selection in animals has been mostly studied in species in which males are signalers and females are choosers. However, in many species, females are (also) signalers. In species with non-signaling females, virgin females are hypothesized to be less choosy than mated females, as virgins must mate to realize fitness and the number of available males is generally limited. Yet, when females signal to attract males, mate limitation can be overcome. We tested how virgin and mated females differ in their calling behavior, mating latency, and in mate choice, using the tobacco budworm Chloridea (Heliothis) virescens as an example for a species in which females are not only choosers but also signalers. We found that virgin females signaled longer than mated females, but virgin and mated signaling females were equally ready to mate, in contrast to non-signaling females. However, we found that virgin signaling females showed weaker mate preference than mated females, which can be explained by the fact that females increase their fitness with multiple matings. Mated females may thus further increase their fitness by more stringent mate selection. We conclude that signaling is a crucial aspect to consider when studying female mate choice because signaling may affect the number of available mates to choose from.

Toward an understanding of the chemical ecology of alternative reproductive tactics in the bulb mite (Rhizoglyphus robini).

BACKGROUND: Under strong sexual selection, certain species evolve distinct intrasexual, alternative reproductive tactics (ARTs). In many cases, ARTs can be viewed as environmentally-cued threshold traits, such that ARTs coexist if their relative fitness alternates over the environmental cue gradient. Surprisingly, the chemical ecology of ARTs has been underexplored in this context. To our knowledge, no prior study has directly quantified pheromone production for ARTs in a male-polymorphic species. Here, we used the bulb mite-in which males are either armed fighters that kill conspecifics, or unarmed scramblers (which have occasionally been observed to induce mating behavior in other males)-as a model system to gain insight into the role of pheromones in the evolutionary maintenance of ARTs. Given that scramblers forgo investment into weaponry, we tested whether scramblers produce higher quantities of the putative female sex-pheromone α-acaridial than fighters, which would improve the fitness of the scrambler phenotype through female mimicry by allowing avoidance of aggression from competitors. To this end, we sampled mites from a rich and a poor nutritional environment and quantified their production of α-acaridial through gas chromatography analysis. RESULTS: We found a positive relationship between pheromone production and body size, but males exhibited a steeper slope in pheromone production with increasing size than females. Females exhibited a higher average pheromone production than males. We found no significant difference in slope of pheromone production over body size between fighters and scramblers. However, scramblers reached larger body sizes and higher pheromone production than fighters, providing some evidence for a potential female mimic strategy adopted by large scramblers. Pheromone production was significantly higher in mites from the rich nutritional environment than the poor environment. CONCLUSION: Further elucidation of pheromone functionality in bulb mites, and additional inter- and intrasexual comparisons of pheromone profiles are needed to determine if the observed intersexual and intrasexual differences in pheromone production are adaptive, if they are a by-product of allometric scaling, or diet-mediated pheromone production under weak selection. We argue chemical ecology offers a novel perspective for research on ARTs and other complex life-history traits.

The stochastic demography of two coexisting male morphs.

Abstract. If genetically distinct morphs coexist under a range of natural conditions, they should have equal long-run fitnesses across a wide range of different stochastic environments. In other words, the sequence and frequency of good and bad environments should not substantially impact long-run growth rates. When different morphs have contrasting life histories that vary with environmental conditions, however, it seems improbable that growth rates can be equivalent across a range of stochastic environments without invoking a strong stabilizing mechanism to explain their persistence. As yet, there has been no research characterizing the long-run stochastic growth rate (lambdaS) of different morphs across a wide range of stochastic environments. Assuming density independence, we show that the two genetic male morphs in the bulb mite (Rhizoglyphus robini-fighters, which are able to kill other mites, and benign scramblers-have similar lambdas in different Markovian environments (different simulated random sequences of good and bad habitats). Elasticity analyses revealed that Xs was most sensitive to perturbation of adult survival rate. A slight (biologically and statistically realistic) increase in scrambler adult survival equalized scrambler and fighter X,. The fitness equivalence of the two morphs suggests that stabilizing mechanisms, such as density or frequency dependence, required to maintain their coexistence, are weak. We advocate that stochastic demography can offer a powerful approach to identify and understand the circumstances under which genetic polymorphisms can be maintained in stochastic environments.

Effects of paternal phenotype and environmental variability on age and size at maturity in a male dimorphic mite.

Investigating how the environment affects age and size at maturity of individuals is crucial to understanding how changes in the environment affect population dynamics through the biology of a species. Paternal phenotype, maternal, and offspring environment may crucially influence these traits, but to my knowledge, their combined effects have not yet been tested. Here, I found that in bulb mites (Rhizoglyphus robini), maternal nutrition, offspring nutrition, and paternal phenotype (males are fighters, able to kill other mites, or benign scramblers) interactively affected offspring age and size at maturity. The largest effect occurred when both maternal and offspring nutrition was poor: in that case offspring from fighter sires required a significantly longer development time than offspring from scrambler sires. Investigating parental effects on the relationship between age and size at maturity revealed no paternal effects, and only for females was its shape influenced by maternal nutrition. Overall, this reaction norm was nonlinear. These non-genetic intergenerational effects may play a complex, yet unexplored role in influencing population fluctuations-possibly explaining why results from field studies often do not match theoretical predictions on maternal effects on population dynamics.

Predation risk increases in estuarine bivalves stressed by low salinity.

Salinity drops in estuaries after heavy rains are expected to increase in frequency and intensity over the next decades, with physiological and ecological consequences for the inhabitant organisms. It was investigated whether low salinity stress increases predation risk on three relevant commercial bivalves in Europe. In laboratory, juveniles of Venerupis corrugata, Cerastoderma edule, and the introduced Ruditapes philippinarum were subjected to low salinities (5, 10 and control 35) during two consecutive days and, afterwards, exposed to one of two common predators in the shellfish beds: the shore crab Carcinus maenas and the gastropod Bolinus brandaris, a non-indigenous species present in some Galician shellfish beds. Two types of choice experiment were done: one offering each predator one prey species previously exposed to one of the three salinities, and the other offering each predator the three prey species at the same time, previously exposed to one of the three salinities. Consumption of both predators and predatory behaviour of C. maenas (handling time, rejections, consumption rate) were measured. Predation rates and foraging behaviour differed, with B. brandaris being more generalist than C. maenas. Still, both predators consumed significantly more stressed (salinity 5 and 10) than non-stressed prey. The overall consumption of the native species C. edule and V. corrugata was greater than that of R. philippinarum, likely due to their vulnerability to low salinity and physical traits (e.g., thinner shell, valve gape). Increasing precipitations can alter salinity gradients in shellfish beds, and thus affect the population dynamics of harvested bivalves via predator-prey interactions. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00227-021-03942-8.