Evolution of Manduca sexta hornworms and relatives: Biogeographical analysis reveals an ancestral diversification in Central America

Kawahara, Akito Y.; Breinholt, Jesse W.; Ponce, Francesca V.; Haxaire, J.; Xiao, Lei; Lamarre, Greg P. A.; Rubinoff, Daniel; Kitching, Ian J.

doi:10.1016/j.ympev.2013.04.017

Cited by 28 publications

(22 citation statements)

References 25 publications

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“…wild and domesticated tobacco). Manduca sexta and its relative the tomato hornworm, Manduca quinquemaculatus , also occur in the ancestral South American range of tomato and in the ancestral centre of domestication for tomato (Mexico; Kawahara et al ., ) and thus may have longer evolutionary history with wild and domesticated tomatoes than our predators. It is unclear how important or abundant M. sexta is across the ranges of various wild tomato species because this natural history data is lacking but, with an ancestral diversification for Manduca probable within Central America and subsequent radiation in North and South America, the co‐occurrence of this herbivore with wild and ancestral tomato is likely (Bai & Lindhout, ; Kawahara et al ., ).…”

Section: Methodsmentioning

confidence: 99%

Domestication of tomato has reduced the attraction of herbivore natural enemies to pest‐damaged plants

Garvey

Kaplan

et al. 2017

Agri and Forest Entomology

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1 Plant domestication can alter species interactions and influence novel associations among crops and insects. We performed a series of preference and performance experiments to test predator and herbivore attraction to domesticated and wild plants and to evaluate the efficacy of herbivore-induced plant volatiles (HIPVs) across a domestication gradient in tomato, including wild relatives, landraces and domesticated commercial cultivars. 2 We employed a tri-trophic system consisting of the specialist lepidopteran herbivore Manduca sexta and two of its natural enemies: an egg predator, the stilt bug Jalysus wickhami, and a larval parasitoid, the wasp Cotesia congregata. 3 In olfactometer trials, natural enemies consistently preferred HIPVs of wild tomatoes over domesticated cultivars, with landraces in between. Plant-domestication effects were also apparent in terms of decision speed: predators were slower to orient towards damaged crops than to damaged wild relatives. 4 By contrast, M. sexta moths were more likely to oviposit on domesticated than on wild or landrace tomatoes, indicating that insect responses to plant odours vary with trophic level. Field trials confirmed olfactory preference tests: caterpillars recovered from wild tomato relatives were more likely to be parasitized than those recovered from landraces or domesticated tomatoes. 5 The results of the present study suggest that tomato domestication has reduced the efficacy of HIPVs in attracting predators compared with wild relatives and also that this decreased attraction leads to lower attack rates by enemies in the field. This outcome has implications for understanding the specificity of tri-trophic plant defences and the compatibility of natural enemies for biocontrol in agro-ecosystems.

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Section: Methodsmentioning

confidence: 99%

Domestication of tomato has reduced the attraction of herbivore natural enemies to pest‐damaged plants

Garvey

Kaplan

et al. 2017

Agri and Forest Entomology

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“…Using RAxML 8.0.24 (42), we estimated phylogenetic trees with ML and ran Bayesian analyses with MrBayes 3.2 (43). We partitioned the dataset in RAxML following PartitionFinder results and applied the GTR+GAMMA model to all partitions and searched for the best tree with the "-f d" option using 200 random starting topologies and a combined bootstrap and likelihood search for 1,000 bootstrap pseudoreplicates with the "-f a" option following our previously published approach (44). For the Bayesian analysis, we followed the same partition scheme as used in RAxML but used PartitionFinder to optimize the models available in MrBayes.…”

Section: Methodsmentioning

confidence: 99%

Moth tails divert bat attack: Evolution of acoustic deflection

Barber

Leavell

Keener

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Adaptations to divert the attacks of visually guided predators have evolved repeatedly in animals. Using high-speed infrared videography, we show that luna moths (Actias luna) generate an acoustic diversion with spinning hindwing tails to deflect echolocating bat attacks away from their body and toward these nonessential appendages. We pit luna moths against big brown bats (Eptesicus fuscus) and demonstrate a survival advantage of ∼47% for moths with tails versus those that had their tails removed. The benefit of hindwing tails is equivalent to the advantage conferred to moths by bat-detecting ears. Moth tails lured bat attacks to these wing regions during 55% of interactions between bats and intact luna moths. We analyzed flight kinematics of moths with and without hindwing tails and suggest that tails have a minimal role in flight performance. Using a robust phylogeny, we find that long spatulate tails have independently evolved four times in saturniid moths, further supporting the selective advantage of this anti-bat strategy. Diversionary tactics are perhaps more common than appreciated in predator-prey interactions. Our finding suggests that focusing on the sensory ecologies of key predators will reveal such countermeasures in prey.antipredator defense | bat-moth interactions | Lepidoptera | Saturniidae P redators are under pressure to perform incapacitating initial strikes to thwart prey escape. It is thought that prey, in turn, have evolved conspicuous colors or markings to deflect predator attack to less vulnerable body regions (1, 2). Eyespots are a wellknown class of proposed deflection marks (3), which are found in a variety of taxa, including Lepidoptera (3) and fishes (4), but only recently have experiments convincingly demonstrated that these color patterns redirect predatory assault. Eyespots on artificial butterfly (5) and fish (4) prey draw strikes of avian and fish predators. Eyespots on the wing margins of woodland brown butterflies (Lopinga achine) lure the attacks of blue tits (Cyanistes caeruleus) (6). Brightly colored lizard tails also divert avian predator attacks to this expendable body region (7).Deflection coloration is unlikely to be an effective strategy against echolocating bats, as these predators have scotopic vision and poor visual acuity unsuited for prey localization and discrimination (8). Most bats rely on echoes from their sonar cries to image prey and other objects in their environment-they live in an auditory world (9). Thus, we would expect a deflection strategy, effective against bats, to present diversionary acoustic signatures to these hearing specialists. Weeks (10) proposed that saturniid hindwing tails might serve to divert bat attacks from essential body parts. We hypothesized that saturniid tails, spinning behind a flying moth (Movie S1) and reflecting sonar calls, serve as either a highly contrasting component of the primary echoic target or as an alternative target. We predicted that bats would aim their attacks at moth tails, instead of the wings or body, durin...

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“…Despite large computational demands, we also managed to conduct a limited number of ML searches that were partitioned by gene. substitution model was applied to the nucleotide dataset for each codon position, and best ML tree searches were conducted using: (i) tree searches starting from a random topology using the '-f d' option (explained further in Kawahara et al [38]) for 100 ML searches and (ii) tree searches using bootstrap trees as starting topologies for 50 ML searches. For amino acids, a single partition was used owing to computational limitations.…”

Section: (B) Phylogenomic Analysismentioning

confidence: 99%

Phylogenomics provides strong evidence for relationships of butterflies and moths

2014

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Butterflies and moths constitute some of the most popular and charismatic insects. Lepidoptera include approximately 160 000 described species, many of which are important model organisms. Previous studies on the evolution of Lepidoptera did not confidently place butterflies, and many relationships among superfamilies in the megadiverse clade Ditrysia remain largely uncertain. We generated a molecular dataset with 46 taxa, combining 33 new transcriptomes with 13 available genomes, transcriptomes and expressed sequence tags (ESTs). Using HaMStR with a Lepidoptera-specific coreorthologue set of single copy loci, we identified 2696 genes for inclusion into the phylogenomic analysis. Nucleotides and amino acids of the all-gene, alltaxon dataset yielded nearly identical, well-supported trees. Monophyly of butterflies (Papilionoidea) was strongly supported, and the group included skippers (Hesperiidae) and the enigmatic butterfly-moths (Hedylidae). Butterflies were placed sister to the remaining obtectomeran Lepidoptera, and the latter was grouped with greater than or equal to 87% bootstrap support. Establishing confident relationships among the four most diverse macroheteroceran superfamilies was previously challenging, but we recovered 100% bootstrap support for the following relationships: ((Geometroidea, Noctuoidea), (Bombycoidea, Lasiocampoidea)). We present the first robust, transcriptome-based tree of Lepidoptera that strongly contradicts historical placement of butterflies, and provide an evolutionary framework for genomic, developmental and ecological studies on this diverse insect order.

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Evolution of Manduca sexta hornworms and relatives: Biogeographical analysis reveals an ancestral diversification in Central America

Cited by 28 publications

References 25 publications

Domestication of tomato has reduced the attraction of herbivore natural enemies to pest‐damaged plants

Domestication of tomato has reduced the attraction of herbivore natural enemies to pest‐damaged plants

Moth tails divert bat attack: Evolution of acoustic deflection

Phylogenomics provides strong evidence for relationships of butterflies and moths

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