Use it or lose it: reproductive implications of ecological specialization in a haematophagous ectoparasite

Using experimentally induced disruptive selection, we tested two hypotheses regarding the evolution of specialization in parasites. The 'trade-off' hypothesis suggests that adaptation to a specific host may come at the expense of a reduced performance when exploiting another host. The alternative 'relaxed selection' hypothesis suggests that the ability to exploit a given host would deteriorate when becoming obsolete. Three replicate populations of a flea Xenopsylla ramesis were maintained on each of two rodent hosts, Meriones crassus and Dipodillus dasyurus, for nine generations. Fleas maintained on a specific host species for a few generations substantially decreased their reproductive performance when transferred to an alternative host species, whereas they generally did not increase their performance on their maintenance host. The results support the 'relaxed selection' hypothesis of the evolution of ecological specialization in haematophagous ectoparasites, while suggesting that trade-offs are unlikely drivers of specialization. Further work is needed to study the extent by which the observed specializations are based on epigenetic or genetic modifications.     

Experimental evolution of the grain of metabolic specialization in yeast

Adaptation to any given environment may be accompanied by a cost in terms of reduced growth in the ancestral or some alternative environment. Ecologists explain the cost of adaptation through the concept of a trade‐off, by which gaining a new trait involves losing another trait. Two mechanisms have been invoked to explain the evolution of trade‐offs in ecological systems, mutational degradation, and functional interference. Mutational degradation occurs when a gene coding a specific trait is not under selection in the resident environment; therefore, it may be degraded through the accumulation of mutations that are neutral in the resident environment but deleterious in an alternative environment. Functional interference evolves if the gene or a set of genes have antagonistic effects in two or more ecologically different traits. Both mechanisms pertain to a situation where the selection and the alternative environments are ecologically different. To test this hypothesis, we conducted an experiment in which 12 experimental populations of wild yeast were each grown in a minimal medium supplemented with a single substrate. We chose 12 different carbon substrates that were metabolized through similar and different pathways in order to represent a wide range of ecological conditions. We found no evidence for trade‐offs between substrates on the same pathway. The indirect response of substrates on other pathways, however, was consistently negative, with little correlation between the direct and indirect responses. We conclude that the grain of specialization in this case is the metabolic pathway and that specialization appears to evolve through mutational degradation.     

Magadi tilapia ecological specialization: filling the early gap in the speciation continuum

Cichlid fish are well known for their high speciation rates, which are usually accompanied by spectacular and rapid diversification in eco‐morphological and secondary sexual traits. This is best illustrated by the famous repeated explosive radiations in the African Great Lakes Tanganyika, Malawi and Victoria, each lake harbouring several hundreds of mostly endemic species. Correspondingly, cichlids diversified very rapidly in many other lakes across their range. Although the larger radiations, unparalleled in vertebrates, are certainly the most intriguing, they are also the most intricate and difficult to address because of their complex nature. This is where smaller, simpler systems may prove to be the most useful. In this issue of Molecular Ecology, Kavembe et al. ( 2016 ) report very recent genetic diversification accompanied by ecological specialization in cichlids of the small and ecologically extreme Lake Magadi, in Kenya. Combining geometric morphometrics, stable isotope analysis, population genomics using RADSeq data and coalescent‐based modelling techniques, the authors characterize the eco‐morphological differences between genetically distinct populations of Magadi tilapia (Alcolapia grahami), which are consistent with the different environmental conditions they experience, and infer their history of divergence. The simplicity of the focal system and the use of a multidisciplinary approach make this work particularly important for our understanding of the early stages of speciation, in both cichlids and other organisms.     

Landscape effects on the thermotolerance of carabid beetles and the role of behavioral thermoregulation

Physiological thermotolerance and behavioral thermoregulation are central to seasonal cold adaptation in ectothermic organisms. For species with enhanced mobility, behavioral responses may be of greater importance in the cold stress response. Employing the carabid beetles as a study organism, the current study compared physiological thermotolerance and behavioral thermoregulation in carabid species inhabiting cereal fields in different landscape contexts, from fine grain heterogeneous “complex” landscapes to homogenous “simple” landscapes. Physiological thermotolerance was determined via measurement of the CT_min and chill coma temperature. Behavioral responses to cold temperature exposure were determined employing a purpose built arena, and thoracic temperature measured to estimate the efficacy of the behavior as a form of behavioral thermoregulation. Results revealed an influence of landscape composition on the cold tolerance of carabid beetles, although species differed in their sensitivity to landscape intensification. A reduced effect of landscape on the thermotolerance of larger carabid beetles was observed, thought to be the consequence of greater mobility preventing local acclimation to microclimatic variation along the landscape intensification gradient. Investigation into behavioral thermoregulation of the 3 largest species revealed burrowing behavior to be the main behavioral response to cold stress, acting to significantly raise carabid body temperature. This finding highlights the importance of behavioral thermoregulation as a strategy to evade cold stress. The use of behavioral thermoregulation may negate the need to invest in physiological thermotolerance, further offering explanation for the lack of landscape effect on the physiological thermotolerance of larger carabids.     

Trade‐offs in the evolution of bumblebee colony and body size: a comparative analysis

Trade‐offs between life‐history traits – such as fecundity and survival – have been demonstrated in several studies. In eusocial insects, the number of organisms and their body sizes can affect the fitness of the colony. Large‐than‐average body sizes as well as more individuals can improve a colony's thermoregulation, foraging efficiency, and fecundity. However, in bumblebees, large colonies and large body sizes depend largely on high temperatures and a large amount of food resources. Bumblebee taxa can be found in temperate and tropical regions of the world and differ markedly in their colony sizes and body sizes. Variation in colony size and body size may be explained by the costs and benefits associated with the evolutionary history of each species in a particular environment. In this study, we explored the effect of temperature and precipitation (the latter was used as an indirect indicator of food availability) on the colony and body size of twenty‐one bumblebee taxa. A comparative analysis controlling for phylogenetic effects as well as for the body size of queens, workers, and males in bumblebee taxa from temperate and tropical regions indicated that both temperature and precipitation affect colony and body size. We found a negative association between colony size and the rainiest trimester, and a positive association between the colony size and the warmest month of the year. In addition, male bumblebees tend to evolve larger body sizes in places where the rain occurs mostly in the summer and the overall temperature is warmer. Moreover, we found a negative relationship between colony size and body sizes of queens, workers, and males, suggesting potential trade‐offs in the evolution of bumblebee colony and body size.     

Behavioral adaptations imply a direct link between ecological specialization and reproductive isolation in a sympatrically diverging ground beetle

Adaptation to a previously unoccupied niche within a single population is one of the most contentious topics in evolutionary biology as it assumes the simultaneous evolution of ecologically selected and preference traits. Here, we demonstrate behavioral adaptation to contrasting hydrological regimes in a sympatric mosaic of Pogonus chalceus beetle populations, and argue that this adaptation may result in nonrandom gene flow. When exposed to experimental inundations, individuals from tidal marshes, which are naturally subjected to frequent but short floods, showed a higher propensity to remain submerged compared to individuals from seasonal marshes that are inundated for several months. This adaptive behavior is expected to decrease the probability that individuals will settle in the alternative habitat, resulting in spatial sorting and reproductive isolation of both ecotypes. Additionally, we show that this difference in behavior is induced by the environmental conditions experienced by the beetles during their nondispersive larval stages. Hence, accidental or forced ovipositioning in the alternative habitat may induce both an increased performance and preference to the natal habitat type. Such plastic traits could play an important role in the most incipient stages of divergence with gene flow.     

Phylogenetic evidence for the evolution of ecological specialization in Timema walking‐sticks

We used phylogenetic and ecological information to study the evolution of host‐plant specialization and colour polymorphism in the genus Timema, which comprises 14 species of walking‐sticks that are subject to strong selection for cryptic coloration on their host‐plants. Phylogenetic analysis indicated that this genus consists of three main lineages. Two of the lineages include highly generalized basal species and relatively specialized distal species, and one of the lineages comprises four specialized species. We tested for phylogenetic conservatism in the traits studied via randomizing host‐plant use, and the four basic Timema colour patterns, across the tips of the phylogeny, and determining if the observed number of inferred changes was significantly low compared to the distribution of numbers of inferred changes expected under the null model. This analysis showed that (1) host‐plant use has evolved nonrandomly, such that more closely related species tend to use similar sets of hosts and (2) colour pattern evolution exhibits considerable lability. Inference of ancestral states using maximum parsimony, under four models for the relative ease of gain and loss of plant hosts or colour morphs, showed that (1) for all models with gains of host‐plants even marginally more difficult than losses, and for most optimizations with gains and losses equally difficult, the ancestral Timema were generalized, feeding on the chaparral plants Ceanothus and Adenostoma and possibly other taxa, and (2) for all models with gains of colour morphs more difficult than losses, the ancestral Timema were polymorphic for colour pattern. Generation of null distributions of inferred ancestral states showed that the maximum‐parsimony inference of host‐plant generalization was most robust for the most speciose of the three main Timema lineages. Ancestral states were also inferred using maximum likelihood, after recoding host‐plant use and colour polymorphism as dichotomous characters. Likelihood analyses provided some support for inference of generalization in host‐plant use at ancestral nodes of the two lineages exhibiting mixtures of generalists and specialists, although levels of uncertainty were high. By contrast, likelihood analysis did not estimate ancestral colour morph patterns with any confidence, due to inferred rates of change that were high with respect to speciation rates. Information from biogeography, floristic history and the timing of diversification of the genus are compatible with patterns of inferred ancestral host‐plant use. Diversification in the genus Timema appears to engender three main processes: (1) increased specialization via loss of host‐plants, (2) retention of the same, single, host‐plant and (3) shifts to novel hosts to which lineages were ‘preadapted’ in colour pattern. Our evidence suggests that the radiation of this genus has involved multiple evolutionary transitions from individual‐level specialization (multiple‐niche polymorphism) to population‐level and species‐level specialization. Ecological studies of Timema suggest that such transitions are driven by diversifying selection for crypsis. This paper provides the first phylogeny‐based evidence for the macroevolutionary importance of predation by generalist natural enemies in the evolution of specialization.     

Selection for increased allocation to offspring number under environmental unpredictability

According to life-history theory, the evolution of offspring size is constrained by the trade-off between allocation of resources to individual offspring and the number of offspring produced. Existing models explore the ecological consequences of offspring size, whereas number is invariably treated simply as an outcome of the trade-off with size. Here I ask whether there is a direct evolutionary advantage of increased allocation to offspring number under environmental unpredictability. Variable environments are expected to select for diversification in the timing of egg hatch and seed germination, yet the dependence of the expression of diversification strategies, and thus parental fitness, on offspring number has not previously been recognized. I begin by showing that well-established sampling theory predicts that a target bethedging diversification strategy is more reliably achieved as offspring number increases. I then use a simulation model to demonstrate that higher offspring number leads to greater geometric mean fitness under environmental uncertainty. Natural selection is thus expected to act directly to increase offspring number under assumptions of environmental unpredictability in season quality.     

High proportion of smaller ranged hummingbird species coincides with ecological specialization across the Americas

Ecological communities that experience stable climate conditions have been speculated to preserve more specialized interspecific associations and have higher proportions of smaller ranged species (SRS). Thus, areas with disproportionally large numbers of SRS are expected to coincide geographically with a high degree of community-level ecological specialization, but this suggestion remains poorly supported with empirical evidence. Here, we analysed data for hummingbird resource specialization, range size, contemporary climate, and Late Quaternary climate stability for 46 hummingbird–plant mutualistic networks distributed across the Americas, representing 130 hummingbird species (ca 40% of all hummingbird species). We demonstrate a positive relationship between the proportion of SRS of hummingbirds and community-level specialization, i.e. the division of the floral niche among coexisting hummingbird species. This relationship remained strong even when accounting for climate, furthermore, the effect of SRS on specialization was far stronger than the effect of specialization on SRS, suggesting that climate largely influences specialization through species'' range-size dynamics. Irrespective of the exact mechanism involved, our results indicate that communities consisting of higher proportions of SRS may be vulnerable to disturbance not only because of their small geographical ranges, but also because of their high degree of specialization.     

Females of the weevil Zabrotes subfasciatus manipulate the size and number of eggs according to the host seed availability

Abstract. In some insects, the finding of oviposition substrate triggers the uptake into oocytes of yolk proteins that are stored in the fat body during post‐embryonic development. The main host of the bean weevil Zabrotes subfasciatus (Coleoptera; Chrysomelidae; Bruchinae; Amblycerini), in which larval resources are the sole source for future egg maturation, is Phaseolus vulgaris. Despite not feeding as adults, females of this species are able to lay eggs after encountering host seeds but it is not known how females react to changes in the availability of bean seeds. In the present study, the behaviour of Z. subfasciatus facing two very different environments for oviposition is investigated, as well as how this influences offspring fitness. The results obtained show that females of Z. subfasciatus react to variations in the availability of seeds belonging to the same host species by adjusting egg size and number. Females on low bean seed density lay larger and fewer eggs than those on high bean seed density, demonstrating a trade‐off between these reproductive traits. Moreover, females can adjust egg size to changing levels of host availability during the first 4 days of their oviposition period. Although no difference in offspring weight is found, those from small eggs (low competition environment) result in larger adults. No response to selection on these traits after rearing beetles on the same host for 40 generations is observed. This unresponsiveness may indicate that beetle populations behave according to their reaction norm that already allows rapid adaptation to a varying amount of host‐seed availability and better exploitation of the environments of this widespread stored‐seed pest.     

Evolution of life‐history traits in geographically isolated populations of Vaejovis scorpions (Scorpiones: Vaejovidae)

Geographical isolation can over time accumulate life‐history variation which can eventually lead to speciation. We used five species of Vaejovis scorpions that have been isolated from one another since the Pleistocene glaciation to identify if biogeographical patterns have allowed for the accumulation of life‐history variation among species. Gravid females were captured and brought back to the lab until giving birth. Once offspring had begun to disperse, measurements of female size, reproductive investment, offspring size, offspring number, and variation in offspring size were recorded. Differences in how each species allocated energy to these variables were analysed utilizing path analysis and structural equation modelling. Female and offspring size, litter size, and total litter mass differed among species, but relative energetic investment did not. Most significant differences among species were not present after removing the effect of female size, indicating that female size is a major source of life‐history variation. Path analyses indicated that there was no size–number trade‐off within any species and that each species allocates energy toward total litter mass differently. Additionally, as offspring size increased, the variation in offspring mass decreased. These results show that each species allocates the same relative amount of energy in different ways. The variation seen could be a response to environmental variability or uncertainty, a product of maternal effects, or caused by the sufficient accumulation of genetic differences due to geographical isolation. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 715–727.     

Testing the role of ecological selection on colour pattern variation in the butterfly Parnassius clodius

Colour pattern has served as an important phenotype in understanding the process of natural selection, particularly in brightly coloured and variable species like butterflies. However, different selective forces operate on aspects of colour pattern, for example by favouring warning colours in eyespots or alternatively favoring investment in thermoregulatory properties of melanin. Additionally, genetic drift influences colour phenotypes, especially in populations undergoing population size change. Here, we investigated the relative roles of genetic drift and ecological selection in generating the phenotypic diversity of the butterfly Parnassius clodius. Genome‐wide patterns of single nucleotide polymorphism data show that P. clodius forms three population clusters, which experienced a period of population expansion following the last glacial maximum and have since remained relatively stable in size. After correcting for relatedness, morphological variation is best explained by climatic predictor variables, suggesting ecological selection generates trait variability. Solar radiation and precipitation are both negatively correlated with increasing total melanin in both sexes, supporting a thermoregulatory function of melanin. Similarly, wing size traits are significantly larger in warmer habitats for both sexes, supporting a Converse Bergmann Rule pattern. Bright red coloration is negatively correlated with temperature seasonality and solar radiation in males, and weakly associated with insectivorous avian predators in univariate models, providing mixed evidence that selection is linked to warning coloration and predator avoidance. Together, these results suggest that elements of butterfly wing phenotypes respond independently to different sources of selection and that thermoregulation is an important driver of phenotypic differentiation in Parnassian butterflies.     

Genetic architecture for normal and novel host-plant use in two local populations of the herbivorous ladybird beetle, Epilachna pustulosa

Trade-offs in host-plant use are thought to promote the evolution of host specificity. However, usually either positive or no genetic correlations have been found. Whereas factors enhancing variation in overall viability have been claimed to mask negative genetic correlations, alternative hypotheses emphasize the sequential changes in genetic correlation in the course of host-range evolution. In this study, the genetic architectures of performances on different hosts were compared in two populations of the herbivorous ladybird beetle, Epilachna pustulosa, using three host plants, one being normal for both, one novel for only one population, and the other novel for both populations. The genetic correlations between larval periods on normal hosts were significantly positive whereas those between normal and novel hosts were not different from zero. There was no evidence for reduced genetic variation on the normal host-plants. These results suggest that the host-range is not restricted by the antagonistic genetic associations among exploitation abilities on different plant species, but rather that selection of different host-plants may improve the coordination between genes responsible for the use of different plants.     

Healthier or bigger? Trade‐off mediating male dimorphism in the black scavenger fly Sepsis thoracica (Diptera: Sepsidae)

1. Life history trade‐offs emerge when limited resources are allocated to multiple functions of an organism. Under highly competitive conditions trade‐offs can result in alternative phenotypes that differ morphologically and physiologically. Such is the case in insect species that grow under high densities, where competition for resources but also the risk of disease contagion is high, prompting important adjustments in immune response and melanic cuticular pigmentation, with consequent sacrifices in other fitness‐related traits. 2. In the present study, the potential trade‐offs between total‐ and active phenoloxidase (PO), body size and body pigmentation in Sepsis thoracica black scavenger flies that show alternative male morphs differing in cuticular pigmentation, and body size were evaluated. 3. As expected, small/dark (obsidian) males showed higher total‐PO activity than larger/orange (amber) males. A negative relationship was found between total‐PO activity and body size in females and obsidian but not amber males, suggesting that growth and immunity are more costly for the former. In contrast, density did not affect PO activity, as predicted by the density‐dependent prophylaxis hypothesis, which had not been tested in dipterans before. However, rearing density did affect the body size negatively in females and amber but not obsidian males, showing that male morph is largely determined by condition‐dependent plasticity rather than genes. 4. This study provides good evidence that trade‐offs between different life‐history traits can result in alternative resource allocation strategies, even within one species. These strategies can produce strikingly different alternative phenotypes, evincing that there is not only one optimal solution to address fitness optimisation.     

The evolution of different maternal investment strategies in two closely related desert vertebrates

We compared egg size phenotypes and tested several predictions from the optimal egg size (OES) and bet‐hedging theories in two North American desert‐dwelling sister tortoise taxa, Gopherus agassizii and G. morafkai, that inhabit different climate spaces: relatively unpredictable and more predictable climate spaces, respectively. Observed patterns in both species differed from the predictions of OES in several ways. Mean egg size increased with maternal body size in both species. Mean egg size was inversely related to clutch order in G. agassizii, a strategy more consistent with the within‐generation hypothesis arising out of bet‐hedging theory or a constraint in egg investment due to resource availability, and contrary to theories of density dependence, which posit that increasing hatchling competition from later season clutches should drive selection for larger eggs. We provide empirical evidence that one species, G. agassizii, employs a bet‐hedging strategy that is a combination of two different bet‐hedging hypotheses. Additionally, we found some evidence for G. morafkai employing a conservative bet‐hedging strategy. (e.g., lack of intra‐ and interclutch variation in egg size relative to body size). Our novel adaptive hypothesis suggests the possibility that natural selection favors smaller offspring in late‐season clutches because they experience a more benign environment or less energetically challenging environmental conditions (i.e., winter) than early clutch progeny, that emerge under harsher and more energetically challenging environmental conditions (i.e., summer). We also discuss alternative hypotheses of sexually antagonistic selection, which arise from the trade‐offs of son versus daughter production that might have different optima depending on clutch order and variation in temperature‐dependent sex determination (TSD) among clutches. Resolution of these hypotheses will require long‐term data on fitness of sons versus daughters as a function of incubation environment, data as yet unavailable for any species with TSD.     

Summary of the morphological and ecological traits of Central European dung beetles

Ecological, morphological and life‐history traits have been increasingly used in community ecology during the last decade. Dung beetles represent a model group of insects frequently used in studies of landscape ecology and grassland management. Their body sizes and nesting behavioral traits are regularly used to help understand ecological processes at the community level. However, information on their seasonal activity, wing morphometry and dung specialization is sparse in published reports, or is simply not available yet. We thus compiled a comprehensive list of the morphological and ecological traits of Central European dung beetles (Geotrupidae, Scarabaeidae and Aphodiidae). We gathered information from published works and, for the first time, took morphometric measurements of wings. We provide a database of 12 traits for all 100 dung beetle species occurring in Central Europe. Most species are not restricted to one specific dung type, and the most frequently used dung types are sheep/goat, cattle and horse dung, which are almost equally exploited by 90, 89 and 87 species, respectively. More than one‐third of all species are active in winter, and the number of active species is the highest in June. The wing morphometry shows a high variation and is largely determined by the family identity; the ratio of elytron length to wing area is the largest in Aphodiidae but the smallest in Geotrupidae. Our database is the first standardized set of information for Central European dung beetles and can be used in future trait‐based studies focusing on the ecology and conservation of these beetles.     

Phenotypic selection and regulation of reproduction in different environments in wild barley

Plasticity of the phenotypic architecture of wild barley, Hordeum spontaneum, was studied in response to water and nutrient stress. Direct and indirect selection on several vegetative and reproductive traits was estimated and path analysis used to reveal how regulating pathways via maternal investment differed between environments. Vegetative traits displayed differential regulating effect on fitness across experimental environments: (1) increase in size was selected for under optimal conditions and under water stress, but not under nutrient stress; (2) allocation to root biomass was selected for under optimal conditions, but it had no effect under nutrient stress and was strongly selected against when water was limiting; (3) delayed onset of reproduction was selected under nutrient limitation whereas earlier onset was selected under water stress. The regulating effect of reproductive traits on final reproductive output also differed across treatments, operating either at the 'early' stage of plant development through varying the number of initiated spikelets per spike (no stress and water stress treatment) or at the 'late' developmental stage adjusting the fertile spikelet weight (no stress and nutrient stress treatment). Reproductive output was regulated via seed abortion under no stress and water stress treatments. Although the underlying mechanism of the regulation through abortion has yet to be discovered, the specific mechanism of abortion under water stress appears to be different from that under optimal conditions. Our results demonstrate that not only is the character architecture in wild barley plastic and sensitive to changing availability of water and nutrients, but the regulating mechanism of maternal investment is also environmentally sensitive.     

Relationships among male sexually selected traits in the bean bug,Riptortus pedestris (Heteroptera: Alydidae)

Current concepts of sexual selection suggest that male reproductive success is determined by multiple sexual traits. As expression and production of multiple sexual traits are frequently associated with each other, positive or negative correlations among multiple sexual traits ensue. These relationships among traits associated with male reproductive success may be crucial in the evolution of male reproductive strategies. Here, we investigate phenotypic relationships among sexually selected traits in the armed bean bug Riptortus pedestris. In this insect, males with a larger body and weapon are more likely to win male–male competitions, and males with a larger weapon or higher courtship rate are more attractive to females. There was a significant positive correlation between body size and weapon size, whereas the courtship rate had significant negative correlations with body size and weapon size. Our results suggested that there was a phenotypic trade‐off between courtship rate and male morphology. In this insect, smaller males may make more effort in courtship behavior as an alternative mating tactic.