scholarly journals Microevolution of Pieris butterfly genes involved in host-plant adaptation along a host-plant community cline

2021 ◽  
Author(s):  
Yu Okamura ◽  
Ai Sato ◽  
Lina Kawaguchi ◽  
Atsushi J. Nagano ◽  
Masashi Murakami ◽  
...  

Herbivorous insects have evolved counteradaptations to overcome the chemical defenses of their host plants. Several of these counteradaptations have been elucidated at the molecular level, in particular for insects specialized on cruciferous host plants. While the importance of these counteradaptations for host plant colonization is well established, little is known about their microevolutionary dynamics in the field. In this study, we examine patterns of host plant use and insect counteradaptation in three Pieris butterfly species across Japan. The larvae of these butterflies express nitrile-specifier protein (NSP) and its paralog major allergen (MA) in their gut to overcome the highly diversified glucosinolate-myrosinase defense system of their cruciferous host plants. Pieris napi and Pieris melete colonize wild Brassicaceae whereas Pieris rapae typically uses cultivated Brassica as a host, regardless of the local composition of wild crucifers. As expected, NSP and MA diversity was independent of the local composition of wild Brassicaceae in P. rapae. In contrast, NSP diversity correlated with local host plant diversity in both species that preferred wild Brassicaceae. P. melete and P. napi both revealed two distinct major NSP alleles, which shaped diversity among local populations, albeit with different evolutionary trajectories. In comparison, MA showed no indication for local adaptation. Altogether, MA appeared to be evolutionary more conserved than NSP, suggesting that both genes play different roles in diverting host plant chemical defense.

2019 ◽  
Author(s):  
Yu Okamura ◽  
Ai Sato ◽  
Natsumi Tsuzuki ◽  
Masashi Murakami ◽  
Hanna Heidel-Fischer ◽  
...  

AbstractAdaptive traits that enable organisms to conquer novel niches and experience subsequent diversification are ecologically and evolutionarily important. The larvae of Pieris butterflies express nitrile-specifier proteins (NSPs), a key innovation for overcoming the glucosinolate (GLS)-myrosinase-based defense system of their Brassicales host-plants. NSPs are a member of the NSP-like gene family, which includes the major allergen (MA) protein, a paralog of NSP with a GLS-disarming function, and a single domain major allergen (SDMA) protein, whose function is unknown. The arms-race between a highly variable host-plant defense system and members of the NSP-like gene family is suggested to mediate diversification in both Pierid butterflies and Brassicales plants. Here, we combined feeding experiments using 25 Brassicaceae plants and five Pieris species with larval transcriptome data to investigate the evolutionary forces acting on NSP-like gene family members associated with patterns of host-plant usage. Although we observed significantly elevated nonsynonymous to synonymous substitution ratios in NSPs, no such pattern was observed in MAs or SDMAs. Furthermore, we found a signature of positive selection of NSP at a phylogenetic branch which reflects different host-plant preferences. Our data indicate that NSPs have evolved in response to shifting preferences for host plants among five Pieris butterflies, whereas MAs and SDMAs appear to have more conserved functions. Our results show that the evolution and functional differentiation of key genes used in host-plant adaptation play a crucial role in the chemical arms-race between Pieris butterflies and their Brassicales host-plants.


Author(s):  
Ombeline Sculfort ◽  
Melanie McClure ◽  
Bastien Nay ◽  
Marianne Elias ◽  
Violaine Llaurens

AbstractChemical defences in animals are both incredibly widespread and highly diverse. Yet despite the important role they play in mediating interactions between predators and prey, extensive differences in the amounts and types of chemical compounds can exist between individuals, even within species and populations. Here we investigate the potential role of environment and development on the chemical defences of warningly coloured butterfly species from the tribe Heliconiini, which can both synthesize and sequester cyanogenic glycosides (CGs). We reared 5 Heliconiini species in captivity, each on a single species-specific host plant as larvae, and compared them to individuals collected in the wild to ascertain whether the variation in CG content observed in the field might be the result of differences in host plant availability. Three of these species were reared as larvae on the same host plant, Passiflora riparia, to further test how species, sex, and age affected the type and amount of different defensive CGs, and how they affected the ratio of synthesized to sequestered compounds. Then, focusing on the generalist species Heliconius numata, we specifically explored variation in chemical profiles as a result of the host plant consumed by caterpillars and their brood line, using rearing experiments carried out on two naturally co-occurring host plants with differing CG profiles. Our results show significant differences in both the amount of synthesized and sequestered compounds between butterflies reared in captivity and those collected in the field. We also found a significant effect of species and an effect of sex in some, but not all, species. We show that chemical defences in H. numata continue to increase throughout their life, likely because of continued biosynthesis, and we suggest that variation in the amount of synthesized CGs in this species does not appear to stem from larval host plants, although this warrants further study. Interestingly, we detected a significant effect of brood lines, consistent with heritability influencing CG concentrations in H. numata. Altogether, our results point to multiple factors resulting in chemical defence variation in Heliconiini butterflies and highlight the overlooked effect of synthesis capabilities, which may be genetically determined to some extent.


2019 ◽  
Vol 286 (1915) ◽  
pp. 20192198 ◽  
Author(s):  
Adam J. Blake ◽  
Matthew C. Go ◽  
Gina S. Hahn ◽  
Hayley Grey ◽  
Samuel Couture ◽  
...  

Insect herbivores exploit plant cues to discern host and non-host plants. Studies of visual plant cues have focused on colour despite the inherent polarization sensitivity of insect photoreceptors and the information carried by polarization of foliar reflectance, most notably the degree of linear polarization ( DoLP ; 0–100%). The DoLP of foliar reflection was hypothesized to be a host plant cue for insects but was never experimentally tested. Here, we show that cabbage white butterflies, Pieris rapae (Pieridae), exploit the DoLP of foliar reflections to discriminate among plants. In experiments with paired digital plant images, P. rapae females preferred images of the host plant cabbage with a low DoLP (31%) characteristic of cabbage foliage over images of a non-host potato plant with a higher DoLP (50%). By reversing the DoLP of these images, we were able to shift the butterflies' preference for the cabbage host plant image to the potato non-host plant image, indicating that the DoLP had a greater effect on foraging decisions than the differential colour, intensity, or shape of the two plant images. Although previously not recognized, the DoLP of foliar reflection is an essential plant cue that may commonly be exploited by foraging insect herbivores.


2008 ◽  
Vol 58 (4) ◽  
pp. 371-388 ◽  
Author(s):  
Irma Wynhoff ◽  
Mark Grutters ◽  
Frank van Langevelde

AbstractObligate myrmecophilous butterfly species, such as Maculinea teleius and M. nausithous that hibernate as caterpillar in nests of the ant species Myrmica scabrinodis and M. rubra respectively, have narrowly defined habitat requirements. One would expect that these butterflies are able to select for sites that meet all their requirements. Both butterfly species occur in habitats where their initial larval resource, the host plant Sanguisorba officinalis, is abundant, while the ant nests are relatively less abundant. With ants in the proximity of a host plant, caterpillars have a chance of being found by their host ant species, while the host plant could become a sink as caterpillars will die when there are no ants close to the host plant. We tested whether females oviposit on host plants in the close proximity of host ants (ant-mediated oviposition) or whether there is random oviposition, using 587 1-m2 plots in and around a nature reserve in The Netherlands where both species were reintroduced. We found that females of both species indeed more often deposit eggs on host plants nearby ants than on host plants without ants. Visits of adult butterflies to plots with the host plant but without the host ants only occurred in years with high butterfly densities. We argue that understanding site selection for oviposition is important for these highly endangered butterfly species with a specialised life cycle, especially after disturbances or reintroductions.


2021 ◽  
Author(s):  
Christine Andeme Ondzighi-Assoume ◽  
Bandana Bhusal ◽  
Adam Traore ◽  
Wilson K Ouma ◽  
Margaret Mmbaga ◽  
...  

Bacterial isolates that enhance plant growth and suppress plant pathogens growth are essential tools for reducing pesticide applications in plant production systems. The objectives of this study were to develop a reliable fluorescence-based technique for labeling bacterial isolates selected as biological control agents (BCAs) to allow their direct tracking in the host-plant interactions, understand the BCA localization within their host plants, and the route of plant colonization. Objectives were achieved by developing competent BCAs transformed with two plasmids, pBSU101 and pANIC-10A, containing reporter genes eGFP and pporRFP, respectively. Our results revealed that the plasmid-mediated transformation efficiencies of antibiotic-resistant competent BCAs identified as PSL, IMC8, and PS were up 84%. Fluorescent BCA-tagged reporter genes were associated with roots and hypocotyls but not with leaves or stems and were confirmed by fluoresence microscopy and PCR analyses in colonized Arabidopsis and sorghum. This fluorescence-based technique's high resolution and reproducibility make it a platform-independent system that allows tracking of BCAs spatially within plant tissues, enabling assessment of the movement and niches of BCAs within colonized plants. Steps for producing and transforming competent fluorescent BCAs, as well as the inoculation of plants with transformed BCAs, localization, and confirmation of fluorescent BCAs through fluorescence imaging and PCR, are provided in this manuscript. This study features host-plant interactions and subsequently biological and physiological mechanisms implicated in these interactions. The maximum time to complete all the steps of this protocol is approximately three months.


PeerJ ◽  
2020 ◽  
Vol 8 ◽  
pp. e10625
Author(s):  
Ai Sato ◽  
Yu Okamura ◽  
Masashi Murakami

Herbivorous insects are thought to have evolved counteradaptations to conquer chemical defenses in their host plants in a stepwise co-evolutionary process. Papilio butterflies use CYP6B gene family members to metabolize furanocoumarins in their Rutaceae or Apiaceae host plants. CYP6Bs have functionally diverged among Papilio species to be able to metabolite diverse types of furanocoumarins in their host plants. In this study, we examined the diversification and selection patterns of CYP6B among nine Papilio species in Japan (eight Rutaceae specialists and one Apiaceae specialist) and their association with host plant spectra and furanocoumarin profiles. We compared host plant spectrum of eight Rutaceae feeding Papilio species and also performed a furanocoumarin profiling of their host plants. In addition, we reconstructed CYP6B gene phylogeny and performed selection analysis based on the transcriptome data of those nine Papilio species. Among Rutaceae-feeding Papilio species, host plant spectrum differences were correlated with their furanocoumarin profiles. However, all tested Papilio species had similar duplicated sets of CYP6B, with no apparent lineage-specific or host plant-specific pattern of CYP6B diversification. Selection analysis showed a signature of positive selection on a CYP6B branch. The positively selected sites located at predicted substrate recognition sites and we also found that these CYP6B genes were observed only in Rutaceae-feeding species. These findings indicate that most CYP6B diversification occurred in ancestral species of these Papilio species, possibly in association with specific host plant chemical defenses and subsequent gene loss due to host specialization. These processes would have shaped the complex diversification patterns of the CYP6B gene family in Papilio butterflies. Our results also show potentially important CYP6B clades among Papilio species which likely to have diverged functions and associated with host plant phytochemicals in ancestral Papilio species.


2019 ◽  
Vol 42 (1) ◽  
pp. 63-68
Author(s):  
Juan Pablo Cancela ◽  
Sasha Vasconcelos

The distribution of butterfly species is limited by availability of larval host plants growing in suitable climatic conditions. The Two-tailed Pasha, Charaxesjasius (Linnaeus, 1767), is a Mediterranean butterfly with only sporadic historical records in Madrid, Spain’s most central province, where the host plant is uncommon and winters are colder than in most parts of the butterfly’s range. We show the first evidence of juvenile stages of the species in two towns of north-central Madrid and compile records of C.jasius from Madrid over the past four decades. Our results suggest that, in the absence of widespread host plants, C.jasius is using suburban ornamental plantings of its host plant to colonise a region which may be becoming more climatically suitable.


2019 ◽  
Vol 70 (2) ◽  
pp. 79-92
Author(s):  
Peter Russell ◽  
Jim Pateman

Various localities in Croatia were visited in 2015, 2016 and 2017 to search for Melitaea ornata Christoph, 1893, which had been reported previously from six locations. Three of these sites were visited in May 2015 and found to be damp meadows and thus most unsuitable for M. ornata. In May 2016 and June 2017, another location (Mt. Sniježnica), given by Koren & Ŝtih (2013) was visited. In 2016, a plant very similar to a known host-plant of M. ornata, Onopordum illyricum L., was found to have been eaten extensively, with copious amounts of larval frass present; however, no larvae were present and no adults seen. In 2017, a male and two females resembling M. ornata were captured at two different locations on this mountain. Also in 2017, a location in the Republic of Bosnia and Herzegovina approximately 8 km southsoutheast of Trebinje (Herzegovina) and 10 km north of Mt. Sniježnica was visited, where a further M. ornata -like female was captured and two egg masses were collected from first year plants of Carduus collinus Waldst. & Kit., the host-plant used by M. ornata in Slovenia. These were returned to the UK and some reared through to adults and confirmed as Melitaea ornata . The butterfly species seen in the Zagreb district, Mt. Sniježnica and Herzegovina are listed.


2020 ◽  
Author(s):  
Adam J. Blake ◽  
Samuel Couture ◽  
Matthew C. Go ◽  
Gerhard Gries

AbstractWhile it is well documented that insects exploit polarized sky light for navigation, their use of reflected polarized light for object detection has been less well studied. Recently, we have shown that the small white butterfly, Pieris rapae, distinguishes between host and non-host plants based on the degree of linear polarization (DoLP) of light reflected from their leaves. To determine how polarized light cues affect host plant foraging by female P. rapae across their entire visual range including the ultraviolet (300-650 nm), we applied photo polarimetry demonstrating large differences in the DoLP of leaf-reflected light among plant species generally and between host and non-host plants specifically. As polarized light cues are directionally dependent, we also tested, and modelled, the effect of approach trajectory on the polarization of plant-reflected light and the resulting attractiveness to P. rapae. Using photo polarimetry measurements of plants under a range of light source and observer positions, we reveal several distinct effects when polarized reflections are examined on a whole-plant basis rather than at the scale of pixels or of entire plant canopies. Most notably from our modeling, certain approach trajectories are optimal for foraging butterflies, or insects generally, to discriminate between plant species on the basis of the DoLP of leaf-reflected light.


PLoS ONE ◽  
2021 ◽  
Vol 16 (1) ◽  
pp. e0245649
Author(s):  
Pawan Kumar ◽  
Tabasum Akhter ◽  
Parul Bhardwaj ◽  
Rakesh Kumar ◽  
Usha Bhardwaj ◽  
...  

Rapid adaptive responses were evident from reciprocal host-plant switches on performance, digestive physiology and relative gene expression of gut serine proteases in larvae of crucifer pest P. brassicae transferred from cauliflower (CF, Brassica oleracea var. botrytis, family Brassicaceae) to an alternate host, garden nasturtium, (GN, Tropaeolum majus L., family Tropaeolaceae) and vice-versa under laboratory conditions. Estimation of nutritional indices indicated that larvae of all instars tested consumed the least food and gained less weight on CF-GN diet (significant at p≤0.05) as compared to larvae feeding on CF-CF, GN-GN and GN-CF diets suggesting that the switch to GN was nutritionally less favorable for larval growth. Nevertheless, these larvae, especially fourth instars, were adroit in utilizing and digesting GN as a new host plant type. In vitro protease assays conducted to understand associated physiological responses within twelve hours indicated that levels and properties of gut proteases were significantly influenced by type of natal host-plant consumed, change in diet as well as larval age. Activities of gut trypsins and chymotrypsins in larvae feeding on CF-GN and GN-CF diets were distinct, and represented shifts toward profiles observed in larvae feeding continuously on GN-GN and CF-CF diets respectively. Results with diagnostic protease inhibitors like TLCK, STI and SBBI in these assays and gelatinolytic zymograms indicated complex and contrasting trends in gut serine protease activities in different instars from CF-GN diet versus GN-CF diet, likely due to ingestion of plant protease inhibitors present in the new diet. Cloning and sequencing of serine protease gene fragments expressed in gut tissues of fourth instar P. brassicae revealed diverse transcripts encoding putative trypsins and chymotrypsins belonging to at least ten lineages. Sequences of members of each lineage closely resembled lepidopteran serine protease orthologs including uncharacterized transcripts from Pieris rapae. Differential regulation of serine protease genes (Pbr1-Pbr5) was observed in larval guts of P. brassicae from CF-CF and GN-GN diets while expression of transcripts encoding two putative trypsins (Pbr3 and Pbr5) were significantly different in larvae from CF-GN and GN-CF diets. These results suggested that some gut serine proteases that were differentially expressed in larvae feeding on different species of host plants were also involved in rapid adaptations to dietary switches. A gene encoding nitrile-specifier protein (nsp) likely involved in detoxification of toxic products from interactions of ingested host plant glucosinolates with myrosinases was expressed to similar levels in these larvae. Taken together, these snapshots reflected contrasts in physiological and developmental plasticity of P. brassicae larvae to nutritional challenges from wide dietary switches in the short term and the prominent role of gut serine proteases in rapid dietary adaptations. This study may be useful in designing novel management strategies targeting candidate gut serine proteases of P. brassicae using RNA interference, gene editing or crops with transgenes encoding protease inhibitors from taxonomically-distant host plants.


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