Evolution of eye development in the darkness of caves: adaptation, drift, or both?

Rétaux, Sylvie; Casañe, Didier

doi:10.1186/2041-9139-4-26

Cited by 117 publications

(90 citation statements)

References 91 publications

(122 reference statements)

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“…Most insights into sensory reduction concern animal eyes, which usually have thousands of sensory neurons and several peripheral processing centres, and energy expenditure, therefore, maybe especially high, while this argument may be much less obvious when a sensory organ with only two sensory neurons is lost. Current research has indicated that natural selection against eye formation is in effect, however, with a possible role also for genetic drift (Klaus et al 2013;Rétaux and Casane 2013). For hearing organs, direct data on energetic costs are lacking so far, but they almost certainly also differ between types of ears.…”

Section: Selective Forces Shaping the Function Of Tympanal Earsmentioning

confidence: 97%

Selective forces on origin, adaptation and reduction of tympanal ears in insects

Strauß

Stumpner

2014

J Comp Physiol A

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Insect ears evolved many times independently. As a consequence, a striking diversity exists in the location, construction and behavioural implementation of ears. In this review, we first summarise what is known about the evolutionary origin of ears and the presumed precursor organs in the various insect groups. Thereafter, we focus on selective forces for making and keeping an ear: we discuss detecting and localising predators and conspecifics, including establishing new "private" channels for intraspecific communication. More advanced aspects involve judging the distance of conspecifics, or assessing individual quality from songs which makes auditory processing a means for exerting sexual selection on mating partners. We try to identify negative selective forces, mainly in the context of energy expenditure for developing and keeping an ear, but also in conjunction with acoustic communication, which incorporates risks like eavesdropping by predators and parasitoids. We then discuss balancing pressures, which might oppose optimising an ear for a specific task (when it serves different functions, for example). Subsequently, we describe various scenarios that might have led to a reduction or complete loss of ears in evolution. Finally, we describe cases of sex differences in ears and potential reasons for their appearance.

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Section: Selective Forces Shaping the Function Of Tympanal Earsmentioning

confidence: 97%

Selective forces on origin, adaptation and reduction of tympanal ears in insects

Strauß

Stumpner

2014

J Comp Physiol A

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“…Together with the case of the gustatory/visual trade-off previously described (Yamamoto et al, 2009), these constitute the only examples to date of a direct link between the development of two sensory organs, involving a pleiotropic effect of these signaling systems, and suggesting indirect selection as an evolutionary driving force underlying the loss of eyes in CF (Jeffery, 2010;Retaux and Casane, 2013). In F2 hybrids, however, we did not observe an inverse correlation between lens and OE size, further suggesting that the developmental trade-off has a multigenic determinism.…”

Section: Specific Considerations Of Cf Developmental Evolution and Phmentioning

confidence: 99%

Sensory evolution in blind cavefish is driven by early embryonic events during gastrulation and neurulation

et al. 2016

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Natural variations in sensory systems constitute adaptive responses to the environment. Here, we compared sensory placode development in the blind cave-adapted morph and the eyed riverdwelling morph of Astyanax mexicanus. Focusing on the lens and olfactory placodes, we found a trade-off between these two sensory components in the two morphs: from neural plate stage onwards, cavefish have larger olfactory placodes and smaller lens placodes. In a search for developmental mechanisms underlying cavefish sensory evolution, we analyzed the roles of Shh, Fgf8 and Bmp4 signaling, which are known to be fundamental in patterning the vertebrate head and are subtly modulated in space and time during cavefish embryogenesis. Modulating these signaling systems at the end of gastrulation shifted the balance toward a larger olfactory derivative. Olfactory tests to assess potential behavioral outcomes of such developmental evolution revealed that Astyanax cavefish are able to respond to a 10 5 -fold lower concentration of amino acids than their surface-dwelling counterparts. We suggest that similar evolutionary developmental mechanisms may be used throughout vertebrates to drive adaptive sensory specializations according to lifestyle and habitat.

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“…; Niven and Laughlin ). A particularly interesting emergent question is whether there is a common morphological mechanism or pattern to this process, or if it is driven randomly by neutral mutation or pleiotropy (Rétaux and Casane ). Eyes are likely to have evolved more than 40 times among animals and take many different forms (von Salvini‐Plawen and Mayr ).…”

mentioning

confidence: 99%

Repeated eye reduction events reveal multiple pathways to degeneration in a family of marine snails

Sumner‐Rooney

Sigwart

McAfee³

et al. 2016

Evolution

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Eye reduction occurs in many troglobitic, fossorial, and deep-sea animals but there is no clear consensus on its evolutionary mechanism. Given the highly conserved and pleiotropic nature of many genes instrumental to eye development, degeneration might be expected to follow consistent evolutionary trajectories in closely related animals. We tested this in a comparative study of ocular anatomy in solariellid snails from deep and shallow marine habitats using morphological, histological, and tomographic techniques, contextualized phylogenetically. Of 67 species studied, 15 lack retinal pigmentation and at least seven have eyes enveloped by surrounding epithelium. Independent instances of reduction follow numerous different morphological trajectories. We estimate eye loss has evolved at least seven times within Solariellidae, in at least three different ways: characters such as pigmentation loss, obstruction of eye aperture, and "lens" degeneration can occur in any order. In one instance, two morphologically distinct reduction pathways appear within a single genus, Bathymophila. Even amongst closely related animals living at similar depths and presumably with similar selective pressures, the processes leading to eye loss have more evolutionary plasticity than previously realized. Although there is selective pressure driving eye reduction, it is clearly not morphologically or developmentally constrained as has been suggested by previous studies.

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Evolution of eye development in the darkness of caves: adaptation, drift, or both?

Cited by 117 publications

References 91 publications

Selective forces on origin, adaptation and reduction of tympanal ears in insects

Selective forces on origin, adaptation and reduction of tympanal ears in insects

Sensory evolution in blind cavefish is driven by early embryonic events during gastrulation and neurulation

Repeated eye reduction events reveal multiple pathways to degeneration in a family of marine snails

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