Evolution of host specificity drives reproductive isolation among RNA viruses

Ecological speciation hypotheses claim that assortative mating evolves as a consequence of divergent natural selection for ecologically important traits. Reproductive isolation is expected to be particularly likely to evolve by this mechanism in species such as phytophagous insects that mate in the habitats in which they eat. We tested this expectation by monitoring the evolution of reproductive isolation in laboratory populations of an RNA virus that undergoes genetic exchange only when multiple virus genotypes coinfect the same host. We subjected four populations of the RNA bacteriophage phi6 to 150 generations of natural selection on a novel host. Although there was no direct selection acting on host range in our experiment, three of the four populations lost the ability to infect one or more alternative hosts. In the most extreme case, one of the populations evolved a host range that does not contain any of the hosts infectible by the wild-type phi6. Whole genome sequencing confirmed that the resulting reproductive isolation was due to a single nucleotide change, highlighting the ease with which an emerging RNA virus can decouple its evolutionary fate from that of its ancestor. Our results uniquely demonstrate the evolution of reproductive isolation in allopatric experimental populations. Furthermore, our data confirm the biological credibility of simple "no-gene" mechanisms of assortative mating, in which this trait arises as a pleiotropic effect of genes responsible for ecological adaptation.     

Continental-scale patterns of Cecropia reproductive phenology: evidence from herbarium specimens

Plant phenology is concerned with the timing of recurring biological events. Though phenology has traditionally been studied using intensive surveys of a local flora, results from such surveys are difficult to generalize to broader spatial scales. In this study, contrastingly, we assembled a continental-scale dataset of herbarium specimens for the emblematic genus of Neotropical pioneer trees, Cecropia, and applied Fourier spectral and cospectral analyses to investigate the reproductive phenology of 35 species. We detected significant annual, sub-annual and continuous patterns, and discuss the variation in patterns within and among climatic regions. Although previous studies have suggested that pioneer species generally produce flowers continually throughout the year, we found that at least one third of Cecropia species are characterized by clear annual flowering behaviour. We further investigated the relationships between phenology and climate seasonality, showing strong associations between phenology and seasonal variations in precipitation and temperature. We also verified our results against field survey data gathered from the literature. Our findings indicate that herbarium material is a reliable resource for use in the investigation of large-scale patterns in plant phenology, offering a promising complement to local intensive field studies.     

Soil temperature drives elevational patterns of reproductive allometry in a biodiversity hotspot

Understanding the geographic patterns of reproductive allocation helps in clarifying the selective forces that shape the reproductive strategies of plants. However, studies on the elevational patterns of reproductive allocation remain limited. Moreover, although soil attributes have long been suspected to drive elevational patterns of reproductive allocation, few studies have explored this relationship. Delaying reproduction and allocating a high proportion of biomass to vegetative organs may be risky for plants living under high-elevation habitats, as these two processes can potentially lead to plant reproductive failure due to the low temperatures and short growing seasons at high elevations. Thus, we hypothesize that reproductive effort will increase with elevation and the elevational pattern of reproductive allocation will be largely driven by soil attributes, given their covariation with elevation. To test these hypotheses, we determined the vegetative and reproductive biomass of individual Impatiens arguta (Balsaminaceae) plants across 12 populations in the Gaoligong Mountains (China), and collected data on soil temperature, nutrients, moisture, and pH for each population. Based on standard major axis regression and linear regression models, we found that (1) both vegetative and reproductive biomass decreased with elevation; (2) all populations demonstrated significant allometric slopes (i.e., linear coefficients of log[reproductive biomass]???log[vegetative biomass] regressions)?>?1; (3) allometric slopes decreased with elevation; and (4) soil temperature was a better predictor of the allometric slope than elevation, i.e., the allometric slope decreased with soil temperature. These results suggest that plant species growing at high elevation invest proportionately more resources to reproduction as an adaptation to low-temperature environments, and reproductive output is heavily dependent on vegetative growth. This study provides the first evidence of soil temperature driving reproductive allocation patterns, which suggests that plant species will favor allocation to growth under increasing soil temperatures with climate warming.

     

A correlation between photosynthetic temperature adaptation and seasonal phenology patterns in the shortgrass prairie

Summary The temperatures at which chlorophyll fluorescence yield is substantially increased and the temperatures at which the quantum yield for CO₂ uptake is irreversibly inhibited were measured for three shortgrass prairie species. The experimental taxa include, a cool season species (Agropyron smithii), a warm season species (Bouteloua gracilis), and a species which grows throughout the cool and warm seasons (Carex stenophylla). Agropyron smithii exhibited lower high temperature damage thresholds (43°C in cool grown plants, 46°C in warm grown plants), relative to the other two species. Bouteloua gracilis exhibited the highest tolerance to high temperature, with threshold values being 44–49°C for cool grown plants and 53–55°C for warm grown plants. Carex stenophylla exhibited threshold values which were intermediate to the other two species (43–47°C for cool grown plants, and 51–53°C for warm grown plants). Seasonal patterns in the fluorescence rise temperatures of field grown plants indicated acclimation to increased temperatures in all three species. The results demonstrate a correlation between the high temperature thresholds for damage to the photosynthetic apparatus, and in situ seasonal phenology patterns for the three species.     

Alteration of seasonal reproductive patterns in mares following superior cervical ganglionectomy.

Oestrous behaviour, ovarian follicular development, ovulation and changes in hair coat were observed in Pony mares which were unoperated, sham-ganglionectomized control or bilaterally superior cervical ganglionectomized. Surgery was performed during the winter anoestrus (1975--1976). Reproductive patterns in all groups were similar during the first breeding season (1976) after operation but in ganglionectomized mares the onset of the next breeding season (date of first ovulation in 1977), the pattern of follicular development, date of first oestrus and pattern of hair coat changes were all significantly delayed relative to those of the non-operated and sham-operated mares in 1976 and 1977 and relative to their own patterns in 1976. These results indicate that the pineal-hypothalamo-pituitary axis may regulate or moderate annual reproductive rhythms in mares.     

Host phenology regulates parasite–host demographic cycles and eco‐evolutionary feedbacks

Parasite–host interactions can drive periodic population dynamics when parasites overexploit host populations. The timing of host seasonal activity, or host phenology, determines the frequency and demographic impact of parasite–host interactions, which may govern whether parasites sufficiently overexploit hosts to drive population cycles. We describe a mathematical model of a monocyclic, obligate‐killer parasite system with seasonal host activity to investigate the consequences of host phenology on host–parasite dynamics. The results suggest that parasites can reach the densities necessary to destabilize host dynamics and drive cycling as they adapt, but only in some phenological scenarios such as environments with short seasons and synchronous host emergence. Furthermore, only parasite lineages that are sufficiently adapted to phenological scenarios with short seasons and synchronous host emergence can achieve the densities necessary to overexploit hosts and produce population cycles. Host‐parasite cycles also generate an eco‐evolutionary feedback that slows parasite adaptation to the phenological environment as rare advantageous phenotypes can be driven extinct due to a population bottleneck depending on when they are introduced in the cycle. The results demonstrate that seasonal environments can drive population cycling in a restricted set of phenological patterns and provide further evidence that the rate of adaptive evolution depends on underlying ecological dynamics.     

Control of malaria-transmitting mosquitoes using gene drives

Gene drives are selfish genetic elements that can be re-designed to invade a population and they hold tremendous potential for the control of mosquitoes that transmit disease. Much progress has been made recently in demonstrating proof of principle for gene drives able to suppress populations of malarial mosquitoes, or to make them refractory to the Plasmodium parasites they transmit. This has been achieved using CRISPR-based gene drives. In this article, I will discuss the relative merits of this type of gene drive, as well as barriers to its technical development and to its deployment in the field as malaria control.This article is part of the theme issue ‘Novel control strategies for mosquito-borne diseases''.     

The reproductive phenology of an Amazonian ant species reflects the seasonal availability of its nest sites

In saturated tropical ant assemblages, reproductive success depends on queens locating and competing for scarce nest sites. Little is known about how this process shapes the life histories of tropical ants. Here I investigate the relationship between nest site availability and an important life history trait, reproductive phenology, in the common Amazonian ant species Allomerus octoarticulatus. A. octoarticulatus is a plant-ant that nests in the hollow, swollen stem domatia on Cordia nodosa. I provide evidence that nest sites are limiting for A. octoarticulatus. Most queens produced by A. octoarticulatus colonies died before locating suitable host plants, and most queens that located hosts died before founding colonies, probably from intraspecific competition among queens for control of host plants. I further show that the reproductive phenology of A. octoarticulatus closely matches the seasonal availability of its nest sites, domatia-bearing C. nodosa saplings. Both the production and flight of A. octoarticulatus reproductives, and the number of C. nodosa saplings available for colonization by ants, peaked from March to May. There was correlative evidence that A. octoarticulatus colonies use temperature as a cue to synchronize their reproduction to the availability of C. nodosa saplings: both the production of reproductives by ant colonies and the number of C. nodosa saplings available for colonization were correlated with temperature, and not with rainfall. All of these results suggest that nest site limitation constrains the reproductive phenology of A. octoarticulatus.     

The sooner the better: reproductive phenology drives ontogenetic trajectories in a temperate squamate (Podarcis muralis)

Understanding variations in individual trajectories is a crucial evolutionary issue. Terrestrial ectotherms from temperate regions typically face thermal constraints and limited activity periods. Developmental conditions (i.e. embryonic life) and reproductive timing (laying date) should induce phenotypic variations and influence subsequent ontogenetic trajectories (growth and survival). We studied these combined influences in an oviparous squamate, the wall lizard (Podarcis muralis), comprising a multiple clutch species with natural variations in laying date for the first clutch. We experimentally manipulated maternal basking opportunities during gravidity (3, 6 or 9 h per day) and incubation temperature (23 or 29 °C). Early laying date positively influenced winter survival in both incubation treatments. Survival was significantly lower in cool than warm‐incubated individuals (14.8% and 73.6%, respectively) because of delayed hatching date and reduced activity period before winter. Individuals from cool incubation temperature were slightly smaller but had a higher body condition and grew faster during the first month of life. Offspring behaviour was driven by complex interactions between gravidity and incubation treatments. Under cool incubation temperature, defensive behaviour was high, independently of gravidity treatment. Warm incubated individuals showed low defensive response except when maternal basking opportunities were restricted to 3 h. Defensive behaviour at birth had a positive influence on survival in cool‐incubated individuals. The results of the present study highlight the long‐term influence of hatching date that integrates female reproductive timing and incubation conditions. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 00, 000–000.     

Feeding patterns revealed host partitioning in a community of frog-biting mosquitoes

1. Resource partitioning is a critical component in competing species that coexist in a community. The biting behaviour of coexisting frog-biting mosquito species associated with a tropical anuran community is investigated. 2. Monthly samplings were taken for 2 years at two study sites in central Sri Lanka to collect frog-biting mosquitoes, anuran abundance, environmental data, and interactions between mosquitoes and anuran hosts. Mosquitoes were collected using mouth-operated aspirators and sound traps broadcasting anuran calls. Mosquitoes were identified using taxonomic keys and DNA barcodes. 3. A total of 1079 frog-biting mosquitoes from four species belonging to two genera were collected [Uranotaenia rutherfordi (5%), Ur. morphotype 1 (67%), Ur. morphotype 2 (21%), and Mansonia uniformis (7%)]. Species-specific interactions between Uranotaenia mosquitoes and their anuran host were found. Uranotaenia morphotype 1, the most common species, was mainly attracted (99%) to Duttaphrynus melanostictus. Uranotaenia rutherfordi was mainly attracted (95%) to Pseudophilautus rus, while Ur. morphotype 2 was attracted (97%) to Polypedates cruciger. These Uranotaenia species are active at different hours at night that correspond to the peak calling activity of their anuran host. Each Uranotaenia species was active at heights that coincide with the calling sites of their host. In contrast, Ma. uniformis was non-specific in host choice and was equally distributed in space and time with respect to host feeding. 4. Here, previously unknown feeding patterns of co-occurring frog-biting mosquito species and their interactions with anurans present in their community are reported, highlighting the existence of complex behavioural patterns of these mosquito communities.     

Field biology of Edessa rufomarginata (Hemiptera: Pentatomidae): phenology, behavior, and patterns of host plant use

Pentatomids may cause direct and indirect damage to important crop plants. Biological and ecological features of phytophagous stink bugs in natural environments, however, remain poorly documented. Here, we provide an ecological account of Edessa rufomarginata De Geer on Caryocar brasiliense (Caryocaraceae) in the Brazilian savanna. The phenology of E. rufomarginata matched that of its host plant, with immatures developing in the wet season simultaneously with the production of vegetative and reproductive plant tissue. Females do not exhibit parental care and lay eggs more frequently on larger plants. Oviposition frequency, however, does not differ between plants with and without flowers/fruits. Nymphs and adults usually feed on stem parts and more rarely on flower buds and fruits. First- and second-instar nymphs remain aggregated, but disperse as third-instar nymphs. Adults and nymphs were more abundant on mature stems of C. brasiliense compared with other plant locations. Ants visiting the plant to search for extrafloral nectar occasionally tap the abdomen of E. rufomarginata nymphs with their antennae to obtain honeydew. This is the first record of trophobiotic interactions between Edessa stinkbugs and ants, and one of the few for heteropterans. The interaction of the stink bug with other natural enemies, such as predaceous Heniartes (Reduviidae), was also observed. Given the pest status of Edessa species for crop plants, additional field studies on host plants, interaction with ants, and natural enemies in native habitats are needed for an effective management of these stink bugs in tropical agricultural systems.     

Cascading reproductive isolation: Plant phenology drives temporal isolation among populations of a host‐specific herbivore

All organisms exist within a complex network of interacting species, thus evolutionary change may have reciprocal effects on multiple taxa. Here, we demonstrate “cascading reproductive isolation,” whereby ecological differences that reduce gene flow between populations at one trophic level affect reproductive isolation (RI) among interacting species at the next trophic level. Using a combination of field, laboratory and common‐garden studies and long‐term herbaria records, we estimate and evaluate the relative contribution of temporal RI to overall prezygotic RI between populations of Belonocnema treatae, a specialist gall‐forming wasp adapted to sister species of live oak (Quercus virginiana and Q. geminata). We link strong temporal RI between host‐associated insect populations to differences between host plant budbreak phenology. Budbreak initiates flowering and the production of new leaves, which are an ephemeral resource critical to insect reproduction. As flowering time is implicated in RI between plant species, budbreak acts as a “multitrophic multi‐effect trait,” whereby differences in budbreak phenology contribute to RI in plants and insects. These sister oak species share a diverse community of host‐specific gall‐formers and insect natural enemies similarly dependent on ephemeral plant tissues. Thus, our results set the stage for testing for parallelism in a role of plant phenology in driving temporal cascading RI across multiple species and trophic levels.     

Host choice promotes reproductive isolation between host races of the larch budmoth Zeiraphera diniana

The chances for sympatric speciation are improved if ecological divergence leads to assortative mating as a by-product. This effect is known in parasites that find mates using host cues, but studies of larch- and pine-feeding races of the larch budmoth (Zeiraphera diniana, Lepidoptera: Tortricidae) suggest it may also occur when mate attraction is via sex pheromones that are independent of habitat. We have previously shown that females releasing pheromones on or near their own host attract more males of their own race than if placed on the alternative host. This host effect would enhance assortative mating provided adults preferentially alight on their native hosts. Here we investigate alighting preferences in natural mixed forest using a novel likelihood analysis of genotypic clusters based on three semidiagnostic allozyme loci. Both larch and pine females show a realized alighting preference for their own host of 86%. The equivalent preferences of males were 79% for the larch race and 85% for the pine race. These preferences are also detectable in small-scale laboratory experiments, where alighting preferences of larch and pine races towards their own hosts were, respectively, 67 and 66% in females and 69 and 63% in males. Pure larch race moths reared in the laboratory had alighting choice similar to moths from natural populations, while hybrids were intermediate, showing that alighting preferences were heritable and approximately additive. The field estimates of alighting preference, coupled with earlier work on mate choice, yield an estimated rate of natural hybridization between sympatric host races of 2.2-3.8% per generation. Divergent alighting choice enhances pheromone-mediated assortative mating today, and is likely to have been an important cause of assortative mating during initial divergence in host use. Because resources are normally 'coarse-grained' in space and time, assortative mating due to ecological divergence may be a more important catalyst of sympatric speciation than generally realized.     

桑寄生植物繁殖物候研究概述

桑寄生植物是一类自身可以进行光合作用的半寄生性灌木, 作为森林和林地的关键性资源可为鸟类等动物分类群提供重要的食物资源和巢址, 并影响当地的生物多样性。桑寄生植物隶属于檀香目, 包括5科88属约1,600种, 除极地、部分高寒和干旱沙漠地区外均有分布。桑寄生植物繁殖物候的研究对于了解“寄主植物-桑寄生植物-传粉/种子散布者系统”中物种相互作用网络的维持机制、生态系统结构的稳定性具有重要意义。本文综述了桑寄生植物在景观、群落和种群尺度上繁殖物候的表现类型, 发现桑寄生植物主要通过繁殖物候异步的方式延长物候期, 维持与传粉/种子散布者持久的互惠关系以保障自身种群的繁衍。该领域经过近年的发展, 已从单一地描述繁殖物候的表现类型到探究系统中寄主植物、传粉/种子散布者以及桑寄生植物自身生物学特性等因素的分析。通过前人的研究发现桑寄生植物繁殖物候对于该系统内相互作用的双方或多方有重要的适应意义, 今后首先应该对桑寄生植物的基础生物学背景进行研究, 然后还应加强实验验证, 进行多因素综合分析等来探讨桑寄生植物繁殖物候的生态学意义。     

Synchronization of gallers with host plant phenology

In addition to various bottom-up effects, the synchronization of herbivores with their host plant phenology determines quality and quantity of food resources and affects the preference–performance linkage and abundance of herbivores. The synchronization has a more critical meaning for such short-lived galling insects as cecidomyiid adults and young aphid stem mothers than for other insects. This review, first, presents general information about gall midges and gall aphids, together with their life history patterns and some ecological attributes. Second, some important topics of galling insect–host plant relation are briefly reviewed. Then, synchronization patterns between gall midge emergence and host plant phenology are analyzed to discuss the adaptive strategies of gall midges and to show how the amount of available food resources is affected by the time lag in synchronization. The spatial distribution pattern and the preference–performance linkage of aphid stem mothers is also discussed in relation to synchronization. Received: October 2, 1998 / Accepted: July 3, 2000     

Host diversity drives parasite diversity: meta‐analytical insights into patterns and causal mechanisms

Statistical correlations of biodiversity patterns across multiple trophic levels have received considerable attention in various types of interacting assemblages, forging a universal understanding of patterns and processes in free‐living communities. Host–parasite interactions present an ideal model system for studying congruence of species richness among taxa as obligate parasites are strongly dependent upon the availability of their hosts for survival and reproduction while also having a tight coevolutionary relationship with their hosts. The present meta‐analysis examined 38 case studies on the relationship between species richness of hosts and parasites, and is the first attempt to provide insights into the patterns and causal mechanisms of parasite biodiversity at the community level using meta‐regression models. We tested the distinct role of resource (i.e. host) availability and evolutionary co‐variation on the association between biodiversity of hosts and parasites, while spatial scale of studies was expected to influence the extent of this association. Our results demonstrate that species richness of parasites is tightly correlated with that of their hosts with a strong average effect size (r= 0.55) through both host availability and evolutionary co‐variation. However, we found no effect of the spatial scale of studies, nor of any of the other predictor variables considered, on the correlation. Our findings highlight the tight ecological and evolutionary association between host and parasite species richness and reinforce the fact that host–parasite interactions provide an ideal system to explore congruence of biodiversity patterns across multiple trophic levels.     

Large-scale patterns of host use by parasites of freshwater fishes

Organisms that are abundant locally in a habitat patch are commonly observed to be frequent regionally, or among patches. In parasites, species present in high numbers in host individuals are also present in many individuals in the host population. On a larger scale, however, when host species are considered as patches, we may expect the opposite pattern because of the cost of producing mechanisms to evade the immune responses of several host species. Thus parasite species exploiting many host species may achieve lower average abundance in their hosts than parasite species exploiting fewer host species. This prediction was tested with data from 188 species of metazoan parasites of freshwater fish, using a comparative approach that controlled for study effort and phylogenetic influences. A negative correlation was found between the number of host species used by parasites and their average abundance in hosts, measured as either prevalence or intensity of infection. There was no evidence that parasite species fall into distinct categories based on abundance patterns, but rather that they fall along a continuum ranging from a generally low abundance in many host species, to a generally high abundance in few host species. These results applied to both ecto- and endoparasites. The pattern observed suggests the existence of a trade-off between how many host species a parasite can exploit and how well it does on average in those hosts.     

The evolution of host use and unusual reproductive strategies in Achrysocharoides parasitoid wasps

We studied host selection and exploitation, two crucial aspects of parasite ecology, in Achrysocharoides parasitoid wasps, which show remarkable host specificity and unusual offspring sex allocation. We estimated a molecular phylogeny of 15 Achrysocharoides species and compared this with host (plant and insect) phylogenies. This tri-trophic phylogenetic comparison provides no evidence for cospeciation, but parasitoids do show phylogenetic conservation of the use of plant genera. Patterns of sequence divergence also suggest that the parasitoids radiated more recently (or evolved much faster) than their insect hosts. Three main categories of brood production occur in parasitoids: (1) solitary offspring, (2) mixed sex broods and (3) separate (split) sex broods. Split sex broods are very rare and virtually restricted to Achrysocharoides, while the other types occur very widely. Our phylogeny suggests that split sex broods have evolved twice and provides evidence for a transition from solitary to mixed sex broods, via split sex broods, as predicted by theory.