Visual inputs to the mushroom body calyces of the whirligig beetle <i>Dineutus sublineatus</i>: Modality switching in an insect

Lin, Chan; Strausfeld, Nicholas J.

doi:10.1002/cne.23092

Cited by 39 publications

(17 citation statements)

References 58 publications

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“…Opsin duplications were predominantly found in species with behaviours often guided by visual cues, and in many of these species (see references), vision has been shown to be the primary cue for such behaviours: flower visitation ( Larinus minutus , Brassicogethes aeneus 51 and Heterochelus sp. 52,53 ), predation (coccinellids 54 , gyrinids 55,56 , Thanasimus formicarius , Carabus granulatus , Metrius contractus ), host plant detection (chrysomelids 57,58 , coccinellids 59 ), and mate recognition (buprestids 60 ). Duplications were notably absent in nocturnal species, with the exception of the nocturnal active predator, Carabus granulatus , which has been shown to possess a number of spectrally distinct photoreceptors 18 .…”

Section: Discussionmentioning

confidence: 99%

Overcoming the loss of blue sensitivity through opsin duplication in the largest animal group, beetles

Sharkey

Fujimoto

Lord

et al. 2017

Sci Rep

163

119

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Opsin proteins are fundamental components of animal vision whose structure largely determines the sensitivity of visual pigments to different wavelengths of light. Surprisingly little is known about opsin evolution in beetles, even though they are the most species rich animal group on Earth and exhibit considerable variation in visual system sensitivities. We reveal the patterns of opsin evolution across 62 beetle species and relatives. Our results show that the major insect opsin class (SW) that typically confers sensitivity to "blue" wavelengths was lost ~300 million years ago, before the origin of modern beetles. We propose that UV and LW opsin gene duplications have restored the potential for trichromacy (three separate channels for colour vision) in beetles up to 12 times and more specifically, duplications within the UV opsin class have likely led to the restoration of "blue" sensitivity up to 10 times. This finding reveals unexpected plasticity within the insect visual system and highlights its remarkable ability to evolve and adapt to the available light and visual cues present in the environment.At the molecular level, the wavelength sensitivity of an animal photoreceptor is determined by the photopigment, comprising an opsin protein bound to a light-absorbing chromophore. Insects commonly possess three opsin proteins (UV, SW and LW) that form photopigments maximally sensitive to ultraviolet (~350 nm), blue (~440 nm) and green (~530 nm) wavelengths, respectively. As insect opsin genes form distinct phylogenetic clades according to their spectral class (UV, SW or LW) the sensitivity ranges of an insect visual system can usually be estimated by the complement of opsin genes present. In some insects photopigment sensitivity has extended outside of this range into the violet (~420 nm) and red (>600 nm) region of the light spectrum through duplications of the SW 1,2 and LW opsins 2,3

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Section: Discussionmentioning

confidence: 99%

Overcoming the loss of blue sensitivity through opsin duplication in the largest animal group, beetles

Sharkey

Fujimoto

Lord

et al. 2017

Sci Rep

163

119

View full text Add to dashboard Cite

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“…Large MBs with developed calyces are therefore not limited to species which rely predominately on olfactory information to navigate in their environment. They can also be found in aquatic beetle species which navigate mainly by vision (Lin and Strausfeld, 2012). It remains to be investigated if the MBs play a role in visual learning in other insect orders as well.…”

Section: Discussionmentioning

confidence: 99%

Different Roles for Honey Bee Mushroom Bodies and Central Complex in Visual Learning of Colored Lights in an Aversive Conditioning Assay

Plath

Entler

Kirkerud

et al. 2017

Front. Behav. Neurosci.

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The honey bee is an excellent visual learner, but we know little about how and why it performs so well, or how visual information is learned by the bee brain. Here we examined the different roles of two key integrative regions of the brain in visual learning: the mushroom bodies and the central complex. We tested bees' learning performance in a new assay of color learning that used electric shock as punishment. In this assay a light field was paired with electric shock. The other half of the conditioning chamber was illuminated with light of a different wavelength and not paired with shocks. The unrestrained bee could run away from the light stimulus and thereby associate one wavelength with punishment, and the other with safety. We compared learning performance of bees in which either the central complex or mushroom bodies had been transiently inactivated by microinjection of the reversible anesthetic procaine. Control bees learned to escape the shock-paired light field and to spend more time in the safe light field after a few trials. When ventral lobe neurons of the mushroom bodies were silenced, bees were no longer able to associate one light field with shock. By contrast, silencing of one collar region of the mushroom body calyx did not alter behavior in the learning assay in comparison to control treatment. Bees with silenced central complex neurons did not leave the shock-paired light field in the middle trials of training, even after a few seconds of being shocked. We discussed how mushroom bodies and the central complex both contribute to aversive visual learning with an operant component.

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“…The upper and lower eyes supply a separate lamina and medulla, relays from which supply a bilobed lobula. A previous description demonstrated that a unique attribute of the upper eye medulla is its relays supplying exclusively the visual calyces of the paired mushroom bodies [11]. Here we describe a further peculiarity of this optic lobe, which is the presence of a lobula plate exclusively serving the lower eye.…”

Section: Introductionmentioning

confidence: 55%

“…Posteriorly, the upper lobe of the lobula appears split into smaller volumes imposed by parallel bundles of axons (Figure 2C,D, arrows). These axons originate from the upper medulla and project inwards to the medial protocerebrum and then to the mushroom body calyces [11]. These observations suggest that in the adult whirligig beetle there are distinct functional differences between the upper aerial eyes and the lower aquatic eyes.…”

Section: Resultsmentioning

confidence: 99%

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A precocious adult visual center in the larva defines the unique optic lobe of the split-eyed whirligig beetle Dineutus sublineatus

Lin

Strausfeld

2013

Front Zool

Self Cite

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IntroductionWhirligig beetles (Coleoptera: Gyrinidae) are aquatic insects living on the water surface. They are equipped with four compound eyes, an upper pair viewing above the water surface and a lower submerged pair viewing beneath the water surface, but little is known about how their visual brain centers (optic lobes) are organized to serve such unusual eyes. We show here, for the first time, the peculiar optic lobe organization of the larval and adult whirligig beetle Dineutus sublineatus.ResultsThe divided compound eyes of adult whirligig beetles supply optic lobes that are split into two halves, an upper half and lower half, comprising an upper and lower lamina, an upper and lower medulla and a bilobed partially split lobula. However, the lobula plate, a neuropil that in flies is known to be involved in mediating stabilized flight, exists only in conjunction with the lower lobe of the lobula. We show that, as in another group of predatory beetle larvae, in the whirligig beetle the aquatic larva precociously develops a lobula plate equipped with wide-field neurons. It is supplied by three larval laminas serving the three dorsal larval stemmata, which are adjacent to the developing upper compound eye.ConclusionsIn adult whirligig beetles, dual optic neuropils serve the upper aerial eyes and the lower subaquatic eyes. The exception is the lobula plate. A lobula plate develops precociously in the larva where it is supplied by inputs from three larval stemmata that have a frontal-upper field of view, in which contrasting objects such as prey items trigger a body lunge and mandibular grasp. This precocious lobula plate is lost during pupal metamorphosis, whereas another lobula plate develops normally during metamorphosis and in the adult is associated with the lower eye. The different roles of the upper and lower lobula plates in supporting, respectively, larval predation and adult optokinetic balance are discussed. Precocious development of the upper lobula plate represents convergent evolution of an ambush hunting lifestyle, as exemplified by the terrestrial larvae of tiger beetles (Cicindelinae), in which activation of neurons in their precocious lobula plates, each serving two large larval stemmata, releases reflex body extension and mandibular grasp.

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Visual inputs to the mushroom body calyces of the whirligig beetle Dineutus sublineatus: Modality switching in an insect

Cited by 39 publications

References 58 publications

Overcoming the loss of blue sensitivity through opsin duplication in the largest animal group, beetles

Overcoming the loss of blue sensitivity through opsin duplication in the largest animal group, beetles

Different Roles for Honey Bee Mushroom Bodies and Central Complex in Visual Learning of Colored Lights in an Aversive Conditioning Assay

A precocious adult visual center in the larva defines the unique optic lobe of the split-eyed whirligig beetle Dineutus sublineatus

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