A life‐cycle approach to species barriers

What maintains reproductive barriers between closely related species is, of course, of fundamental interest to a closer understanding of the mechanisms that generate new biodiversity. One important dichotomy is to separate barriers evolved from divergent selection over environmental gradients (extrinsic barriers) from barriers caused by incompatibilities between different genetic arrangements that may have evolved in isolation (intrinsic barriers). This dichotomy also reflects an important applied consequence. As the extrinsic barriers are associated with specific environmental contexts, they may be partly or completely erased if the environment changes. In contrast, intrinsic barriers are inert to the environmental context and resistant to environmental changes. From a conservation biology perspective, it may thus be important to be able to separate extrinsic and intrinsic species barriers, but this may in many organisms be a complex matter. In this issue of Molecular Ecology, Montecinos et al. ( 2017 ) found a tractable approach that works for species with life cycles that include two reproductive but ecologically similar generations, one haploid and the other diploid. What they demonstrate is that using a life‐cycle approach offers a unique possibility to separate between prezygotic and postzygotic barriers. Indeed, in the case of an isomorphic life cycle, there is even a possibility to suggest whether postzygotic barriers are more likely to be intrinsic or extrinsic. In this way, their approach may be useful both to increase our understanding of the basic mechanisms of speciation and to single out when species barriers will better resist environmental changes.     

Intra‐specific variability and plasticity influence potential tree species distributions under climate change

Aim To assess the effect of local adaptation and phenotypic plasticity on the potential distribution of species under future climate changes. Trees may be adapted to specific climatic conditions; however, species range predictions have classically been assessed by species distribution models (SDMs) that do not account for intra‐specific genetic variability and phenotypic plasticity, because SDMs rely on the assumption that species respond homogeneously to climate change across their range, i.e. a species is equally adapted throughout its range, and all species are equally plastic. These assumptions could cause SDMs to exaggerate or underestimate species at risk under future climate change. Location The Iberian Peninsula. Methods Species distributions are predicted by integrating experimental data and modelling techniques. We incorporate plasticity and local adaptation into a SDM by calibrating models of tree survivorship with adaptive traits in provenance trials. Phenotypic plasticity was incorporated by calibrating our model with a climatic index that provides a measure of the differences between sites and provenances. Results We present a new modelling approach that is easy to implement and makes use of existing tree provenance trials to predict species distribution models under global warming. Our results indicate that the incorporation of intra‐population genetic diversity and phenotypic plasticity in SDMs significantly altered their outcome. In comparing species range predictions, the decrease in area occupancy under global warming conditions is smaller when considering our survival–adaptation model than that predicted by a ‘classical SDM’ calibrated with presence–absence data. These differences in survivorship are due to both local adaptation and plasticity. Differences due to the use of experimental data in the model calibration are also expressed in our results: we incorporate a null model that uses survival data from all provenances together. This model always predicts less reduction in area occupancy for both species than the SDM calibrated with presence–absence. Main conclusions We reaffirm the importance of considering adaptive traits when predicting species distributions and avoiding the use of occurrence data as a predictive variable. In light of these recommendations, we advise that existing predictions of future species distributions and their component populations must be reconsidered.     

Parasitism and constitutive defence costs to host life‐history traits in a parasitoid–host interaction

1. The level of an organism's investment in defences against natural enemies depends on the fitness costs of resisting parasitism and on the costs of maintaining defences in the absence of infection. Heritable variation in resistance suggests that costs exist, but very little is known about the nature or magnitude of these costs in natural populations of animals. 2. A powerful technique for identifying trade‐offs between fitness components is the study of correlated responses to artificial selection. We selected for increased resistance in the Indian meal moth, Plodia interpunctella, following parasitism by the koinobiont parasitoid, Venturia canescens, and measured the cost of resistance to parasitism and the cost of maintaining resistance in the absence of immune challenge during the next generation. 3. Parasitism decreased larval host size, growth, and developmental time and was significantly negatively correlated with the size of surviving host adults. Larvae of the next generation also had a reduced developmental period, whilst the duration of the invulnerable pupal instar was increased. There was no effect on host adult size and related fecundity in the F₁ generation.     

Family‐level variation in early life‐cycle traits of kelp

Temperate kelp forests (Laminarians) are threatened by temperature stress due to ocean warming and photoinhibition due to increased light associated with canopy loss. However, the potential for evolutionary adaptation in kelp to rapid climate change is not well known. This study examined family‐level variation in physiological and photosynthetic traits in the early life‐cycle stages of the ecologically important Australasian kelp Ecklonia radiata and the response of E. radiata families to different temperature and light environments using a family × environment design. There was strong family‐level variation in traits relating to morphology (surface area measures, branch length, branch count) and photosynthetic performance (F_v/F_m) in both haploid (gametophyte) and diploid (sporophyte) stages of the life‐cycle. Additionally, the presence of family × environment interactions showed that offspring from different families respond differently to temperature and light in the branch length of male gametophytes and oogonia surface area of female gametophytes. Negative responses to high temperatures were stronger for females vs. males. Our findings suggest E. radiata may be able to respond adaptively to climate change but studies partitioning the narrow vs. broad sense components of heritable variation are needed to establish the evolutionary potential of E. radiata to adapt under climate change.     

Selection on flowering time in a life‐cycle context

The main way in which plants can exert control over their local environment is by the timing of different events within their life cycles. Regarding timing of flowering as an integrated part of both the annual cycle and of the whole life cycle, rather than as an isolated event, has important implications for how we assess selection on timing of reproduction and interpret existing phenological patterns in perennial plants. I argue that: 1) we have little unequivocal evidence of pollinator‐mediated selection on flowering time, but perhaps more evidence of antagonist‐mediated selection; 2) much of selection on flowering time might occur before flowers have developed and after reproduction; 3) vital rates of non‐flowering individuals can influence the strength and direction of selection on flowering time, and 4) differences in the direction of selection on flowering date between years might well correspond to consistent selection on the mechanisms determining flowering time. Overall, a life cycle perspective on timing of flowering is likely to facilitate the identification of selective agents and the understanding of the complex mechanisms underlying spatial and temporal variation in selection as well as to enable more accurate predictions of responses to environmental change.     

Effects of diet and host access on fecundity and lifespan in two fruit fly species with different life‐history patterns

The reproductive ability of female tephritids can be limited and prevented by denying access to host plants and restricting the dietary precursors of vitellogenesis. The mechanisms underlying the delayed egg production in each case are initiated by different physiological processes that are anticipated to have dissimilar effects on lifespan and reproductive ability later in life. The egg‐laying abilities of laboratory‐reared females of the Mediterranean fruit fly (Ceratitis capitata Wiedmann) and melon fly (Bactrocera cucurbitae Coquillett) from Hawaii are delayed or suppressed by limiting access to host fruits and dietary protein. In each case, this is expected to prevent the loss of lifespan associated with reproduction until protein or hosts are introduced. Two trends are observed in each species: first, access to protein at eclosion leads to a greater probability of survival and a higher reproductive ability than if it is delayed and, second, delayed host access reduces lifetime reproductive ability without improving life expectancy. When host access and protein availability are delayed, the rate of reproductive senescence is reduced in the medfly, whereas the rate of reproductive senescence is generally increased in the melon fly. Overall, delaying reproduction lowers the fitness of females by constraining their fecundity for the remainder of the lifespan without extending the lifespan. © 2013 The Royal Entomological Society     

Geographical variation in host use of a blood-feeding ectoparasitic fly: implications for population invasiveness

Invasive generalist ectoparasites provide a tool to study factors affecting expansion rates. An increase in the number of host species may facilitate geographic range expansion by increasing the number of suitable habitats and by affecting local extinction and colonization rates. A geographic perspective on parasite host specificity and its implications on range expansion are, however, insufficiently understood. We conducted a field study to explore if divergent host specificity could explain the observed variation in expansion rates between Fennoscandian populations of the deer ked (Lipoptena cervi), which is a blood-feeding ectoparasitic fly of cervids. We found that the rapidly expanding eastern population in Finland appears to specialize on moose, whereas the slowly expanding western population in Norway breeds successfully on both moose and roe deer. The eastern population was also found to utilize the wild forest reindeer as an auxiliary host, but this species is apparently of low value for L. cervi in terms of adult maintenance, reproductive output and offspring quality. Abundant numbers of roe deer and white-tailed deer were observed to be apparently uninfected in Finland, suggesting that host use is not a plastic response to host availability, but rather a consequence of population-level evolutionary changes. Locally compatible hosts were found to be the ones sharing a long history with the deer ked in the area. Cervids that sustained adult deer keds also allowed successful reproduction. Thus, host use is probably determined by the ability of the adult to exploit particular host species. We conclude that a wide host range alone does not account for the high expansion rate or wide geographic distribution of the deer ked, although loose ecological requirements would increase habitat availability.     

Coevolution of an avian host and its parasitic cuckoo

Abstract We use a quantitative genetic model to examine the coevolution of host and cuckoo egg characters (termed "size" as a proxy for general appearance), host discrimination, and host and cuckoo population dynamics. A host decides whether to discard an egg using a comparison of the sizes of the eggs in her nest, which changes as host and cuckoo eggs evolve. Specifically, we assume that the probability that she discards the largest egg in her nest depends on how much larger it is than the second largest egg. This decision rule (i.e., the acceptable difference in egg sizes) also evolves, changing both the chance of successful rejection of a cuckoo egg in parasitized nests and the chance of mistaken rejection of a host egg in both parasitized and unparasitized nests. We find a stable equilibrium for coexistence of the host and cuckoo where there is cuckoo egg mimicry, evolutionary displacement of the host egg away from the cuckoo egg phenotype, and host discrimination against unusual eggs. Both host discrimination and host egg displacement are fairly weak at the equilibrium. Cuckoo egg mimicry, although imperfect, usually evolves more extensively and quickly than the responses of the host. Our model provides evidence for both the evolutionary equilibrium and evolutionary lag hypotheses of host acceptance of parasitic eggs.     

Sex‐biased transmission of a complex life‐cycle parasite: why males matter

Male‐bias in parasite infection exists in a variety of host–parasite systems, but the epidemiological importance of males and, specifically, whether males are responsible for producing a disproportionate amount of onward transmission events (male‐biased transmission) has seldom been tested. The primary goal of our study was to experimentally test for male‐biased transmission in a system with no sex‐biased prevalence. We performed a longitudinal field experiment and continuously removed intestinal nematode parasites from either male or female white‐footed mice and recorded the subsequent transmission among the untreated sex. We predicted males are responsible for the majority of transmission and female mice would have lower infection prevalence under the male‐anthelmintic treatment than controls and that male mice would experience little or no change in infection prevalence under female‐anthelmintic treatment compared to controls. Our second goal was to evaluate physiological hypotheses relating to the mechanisms that could generate the observed transmission pattern. To that end, we examined a cross‐sectional sample of hosts to explicitly test for differences in parasite intensity, parasite egg shedding rate and reproductive output per parasite between male and female hosts. Removing parasites from male mice resulted in lower infection rates among female mice but, in contrast, there was no effect of female‐deworming on infection rates among male mice; providing evidence that males provide disproportionately greater numbers of transmission events than females. We found no difference in prevalence, intensity, or fecundity of parasites between sexes in the cross‐sectional sample of mice and rejected the mechanistic hypotheses. Without male‐biased prevalence, intensity, or parasite fecundity, we concluded that male‐biased transmission is unlikely to be created via physiological differences and the parsimonious explanation is that male behavior spreads infective stages in a more successful manner. We demonstrate that transmission heterogeneities can exist in the absence of individual heterogeneities in infection.     

Frequency‐dependent and density‐dependent larval competition between life‐history strains of a fly,Lucilia cuprina

1. Competition was created between the larvae of two life‐history strains of the blowfly Lucilia cuprina (Wiedemann) that have different requirements for larval resource acquisition. Adult females of one strain had the ability to mature eggs in the absence of adult feeding (autogeny) whereas the other strain lacked this ability. Autogeny shifts the burden of resource acquisition from adults to larvae, potentially leading to greater competition at this earlier life history stage. 2. A replacement series was used to determine the per‐capita competitive effect between strains relative to the intra‐strain effect, and density‐ and frequency‐dependent variation in this per‐capita effect was then evaluated. Evidence was found of competitive superiority of autogenous larvae when they occurred at a low frequency and low density, but their competitive ability was lost or reversed at higher frequencies and densities. 3. A dynamic competitive environment created by frequency and density dependence can account for the maintenance of genetic diversity for major life‐history traits. Such competition may explain why autogeny is rare in field populations of L. cuprina even although underlying genetic variation for the trait seems to be present.     

Intra‐ and interclonal phenotypic and genetic variability of the trematode Maritrema novaezealandensis

Explaining the origin and maintenance of phenotypic variation remains a central challenge in evolutionary biology. Using the trematode parasite Maritrema novaezealandensis, we examined variability in several morphological, behavioural, and physiological phenotypic traits at the same time as controlling for genotype by using genetically identical parasite clonal lineages. We measured several morphological traits, photoreactive responses, and survivorship to quantify the amount of phenotypic variation within and among 42 clonal parasite lines. Additionally, we tested Lerner's hypothesis that homozygotes are more variable than heterozygotes and assessed correlations between heterozygosity and phenotypic variation among clones. We found substantial differences among clones in morphology, photoreactive behaviour, and survivorship, yet no significant differences among clones in levels of intraclonal phenotypic variability were seen. Although the results demonstrate that conspecific trematode clones have significantly different levels of phenotypic variability, consistent differences over time were not always apparent. Finally, no correlation was found between heterozygosity and phenotypic variation among clones and the pattern of highly variable homozygotes, as observed by Lerner, was not evident in the present study. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 106–116.     

Evolution of larval competitiveness and associated life‐history traits in response to host shifts in a seed beetle

Resource competition is frequently strong among parasites that feed within small discrete resource patches, such as seeds or fruits. The properties of a host can influence the behavioural, morphological and life‐history traits of associated parasites, including traits that mediate competition within the host. For seed parasites, host size may be an especially important determinant of competitive ability. Using the seed beetle, Callosobruchus maculatus, we performed replicated, reciprocal host shifts to examine the role of seed size in determining larval competitiveness and associated traits. Populations ancestrally associated with either a small host (mung bean) or a large one (cowpea) were switched to each other's host for 36 generations. Compared to control lines (those remaining on the ancestral host), lines switched from the small host to the large host evolved greater tolerance of co‐occurring larvae within seeds (indicated by an increase in the frequency of small seeds yielding two adults), smaller egg size and higher fecundity. Each change occurred in the direction predicted by the traits of populations already adapted to cowpea. However, we did not observe the expected decline in adult mass following the shift to the larger host. Moreover, lines switched from the large host (cowpea) to the small host (mung bean) did not evolve the predicted increase in larval competitiveness or egg size, but did exhibit the predicted increase in body mass. Our results thus provide mixed support for the hypothesis that host size determines the evolution of competition‐related traits of seed beetles. Evolutionary responses to the two host shifts were consistent among replicate lines, but the evolution of larval competition was asymmetric, with larval competitiveness evolving as predicted in one direction of host shift, but not the reverse. Nevertheless, our results indicate that switching hosts is sufficient to produce repeatable and rapid changes in the competition strategy and fitness‐related traits of insect populations.     

Intra‐specific body size variation in Polistes paper wasps as a response to social parasite pressure

1. Like avian brood parasites, obligate insect social parasites exploit the parental care of a host species to rear their brood, causing an evident loss of host reproductive success. This fitness cost imposes selective pressure on the host to reduce the parasite effect. A possible outcome of an evolutionary arms race is the selection of host morphological counter‐adaptations to resist parasite attacks. 2. We studied host–parasite pairs of Polistes wasps in which the fighting equipment of the parasite's body allows it to enter the host colony. 3. We searched for host morphological traits related to fighting ability that could be considered counter‐adaptations. As a host–parasite co‐evolutionary arms race can only occur where the two lineages co‐exist, we compared morphological traits of hosts belonging to populations with or without parasite pressure. We report that host foundresses belonging to populations under strong parasite pressure have a larger body size than those belonging to populations without parasite pressure. 4. Behavioural experiments carried out to test if an increase in host body size is useful to oppose parasite usurpation show that large body size foundresses exhibit a greater ability of nest defence.     

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

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

Influences of two life‐history stages of the weevil,Larinus minutus,on its host plant Centaurea diffusa

1. We hypothesised that, for weed biological control, using species that feed as both adults and larvae would be advantageous. Here, we test the impacts of adult and larval feeding of Larinus minutus (Col.: Curculionidae), a successful biological control agent of diffuse knapweed, Centaurea diffusa (Asteraceae), in British Columbia, Canada. 2. At one site, the observations of the present study showed that the intensity of adult weevil feeding did not predict the level of larval attack. Experiments found no evidence for plant‐mediated competition between the life‐history stages. 3. At two sites and in two years, experimental manipulations of adult and/or larval feeding damage were conducted and plant performance measured. Neither antagonistic nor synergistic interactions occurred, but at each of the two sites a different life‐history stage was responsible for reduction in the number of seeds produced by the plants. 4. Although one of the two different feeding modes was redundant at each site, the ability of adults and larvae to reduce plant performance in different areas makes the species effective in a wider range of environments.     

Experimental analysis of an early life‐history stage: avian predation selects for larger body size of hatchling turtles

One common life‐history pattern involves an elevated rate and nonrandom distribution of neonatal mortality. However, the mechanisms causing this pattern and the specific traits that confer a survival benefit are not always evident. We conducted a manipulative field experiment using red‐eared slider turtles to test the hypothesis that diurnal avian predators are a primary cause of size‐specific neonatal mortality. Body size was a significant predictor of recapturing hatchlings alive and of finding hatchlings dead under natural conditions, but was unimportant when diurnal predators were excluded from the field site. Overall recapture rates also more than doubled when predators were excluded compared to natural conditions (72.4 vs. 34.9%). We conclude that birds are an important cause of size‐specific mortality of recently emerged hatchling turtles and that ‘bigger is better’ in this system, which has important implications for life‐history evolution in organisms that experience size‐specific neonatal mortality.     

Intra‐specific variability in Rhinoleucophenga punctulata populations (Diptera: Drosophilidae) from Neotropical biomes: Combined analyses of morphological and molecular data

Despite the fact that Drosophilidae is a very diverse and well‐studied taxon, the New World genus Rhinoleucophenga is yet poorly understood even in regard to species distribution and morphological variability pattern. In this sense, R. punctulata is a species widely distributed in the Neotropical region. Specimens of R. punctulata were collected from different biomes in Brazil: Pampa, Cerrado and Caatinga sensu strictu, and a southern Amazonian savannah enclave area. Geographical variations in the external body morphology and in the morphology of spermatheca were noticed among the different populations. The hypothesis that each population could be a different species was tested through molecular data. A fragment of the mitochondrial cytochrome c oxydase subunit I (COI) gene was sequenced to perform phylogenetic analyses through neighbor‐joining and Bayesian inferences. Pairwise genetic divergences of COI sequences were calculated using DNA barcode premises. The analyzed populations presented different variation levels in both morphology and molecular traits. However, new species were not proposed because the intra‐population nucleotide variations exceeded the inter‐population ones. The noticeable morphological and genetic variations revealed among the four studied populations of R. punctulata in different biomes of Brazil suggest the necessity that morphological, distributional and molecular data at the population level should be integrated into complementary datasets to better understand the biological diversity of Rhinoleucophenga through Neotropical environments.     

Intraspecific variability in egg maturation patterns and associated life‐history trade‐offs in a polyembryonic parasitoid wasp

1. Life‐history theory predicts a trade‐off between the resources allocated to reproduction and those allocated to survival. Early maturation of eggs (pro‐ovigeny) is correlated with small body size and low adult longevity in interspecific comparisons among parasitoids, demonstrating this trade‐off. The handful of studies that have tested for similar correlations within species produced conflicting results. 2. Egg maturation patterns and related life‐history traits were studied in the polyembryonic parasitoid wasp, Copidosoma koehleri (Hymenoptera: Encyrtidae). Although the genus Copidosoma was previously reported to be fully pro‐ovigenic, mean egg loads of host‐deprived females almost doubled within their first 6 days of adulthood. 3. The initial egg‐loads of newly emerged females were determined and age‐specific realised fecundity curves were constructed for their clone‐mate twins. The females' initial egg loads increased with body size, but neither body size nor initial egg load was correlated with longevity and fecundity. 4. The variation in initial egg loads was lowest among clone‐mates, intermediate among non‐clone sisters and highest among non‐sister females. The within‐clone variability indicates environmental influences on egg maturation, while the between‐clone variation may be genetically based. 5. Ovaries of host‐deprived females contained fewer eggs at death (at ～29 days) than on day 6. Their egg loads at death were negatively correlated with life span, consistent with reduced egg production and/or egg resorption. Host deprivation prolonged the wasps' life span, suggesting a survival cost to egg maturation and oviposition. 6. It is concluded that adult fecundity and longevity were not traded off with pre‐adult egg maturation.