Behavioral evidence for cone-based ultraviolet vision in divergent bat species and implications for its evolution

Xuan, Fujun; Hu, Kongxin; Zhu, Tengteng; Paul, Racey; Wang, Xuzhong; Yi, Sun Shin

doi:10.1590/s1984-46702012000200002

Cited by 8 publications

(8 citation statements)

References 22 publications

(42 reference statements)

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“…2009; Zhao, Ru, et al. 2009; Wu, Wang, and Hadly 2017), behavioral (Fujun et al. 2012), and immunocytochemical studies of the visual pigments (Müller and Peichl 2005; Müller, Goodman, and Peichl 2007) have revealed that earlier expectations of blindness or pure rod retinas in bats (Peichl 2005) were incorrect.…”

Section: Discussionmentioning

confidence: 99%

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As Blind as a Bat? Opsin Phylogenetics Illuminates the Evolution of Color Vision in Bats

Simões

Foley

Hughes

et al. 2018

Molecular Biology and Evolution

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Through their unique use of sophisticated laryngeal echolocation bats are considered sensory specialists amongst mammals and represent an excellent model in which to explore sensory perception. Although several studies have shown that the evolution of vision is linked to ecological niche adaptation in other mammalian lineages, this has not yet been fully explored in bats. Recent molecular analysis of the opsin genes, which encode the photosensitive pigments underpinning color vision, have implicated high-duty cycle (HDC) echolocation and the adoption of cave roosting habits in the degeneration of color vision in bats. However, insufficient sampling of relevant taxa has hindered definitive testing of these hypotheses. To address this, novel sequence data was generated for the SWS1 and MWS/LWS opsin genes and combined with existing data to comprehensively sample species representing diverse echolocation types and niches (SWS1 n = 115; MWS/LWS n = 45). A combination of phylogenetic analysis, ancestral state reconstruction, and selective pressure analyses were used to reconstruct the evolution of these visual pigments in bats and revealed that although both genes are evolving under purifying selection in bats, MWS/LWS is highly conserved but SWS1 is highly variable. Spectral tuning analyses revealed that MWS/LWS opsin is tuned to a long wavelength, 555–560 nm in the bat ancestor and the majority of extant taxa. The presence of UV vision in bats is supported by our spectral tuning analysis, but phylogenetic analyses demonstrated that the SWS1 opsin gene has undergone pseudogenization in several lineages. We do not find support for a link between the evolution of HDC echolocation and the pseudogenization of the SWS1 gene in bats, instead we show the SWS1 opsin is functional in the HDC echolocator, Pteronotus parnellii. Pseudogenization of the SWS1 is correlated with cave roosting habits in the majority of pteropodid species. Together these results demonstrate that the loss of UV vision in bats is more widespread than was previously considered and further elucidate the role of ecological niche specialization in the evolution of vision in bats.

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Section: Discussionmentioning

confidence: 99%

“…Increased interaction with other sensory systems (e.g., olfaction, hearing) may also reduce the impact of SWS1 opsin loss on species’ survival (Zhao, Rossiter, et al. 2009; Fujun et al. 2012; Jacobs 2013).…”

Section: Introductionmentioning

confidence: 99%

As Blind as a Bat? Opsin Phylogenetics Illuminates the Evolution of Color Vision in Bats

Simões

Foley

Hughes

et al. 2018

Molecular Biology and Evolution

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“…This pattern holds for changes in sensory ecology. The evolution of activity under lower light conditions is associated with decreases in visual processing tissue (Barton, Purvis & Harvey, ; Catania, ; Fujun et al ., ; O'Donnell et al ., ). We hypothesize that the evolution of parasitism will lead to reduced brain investment when parasites exploit host sensory and cognitive systems.…”

Section: Introductionmentioning

confidence: 97%

Evidence for adaptive brain tissue reduction in obligate social parasites (Polyergus mexicanus) relative to their hosts (Formica fusca)

Sulger

McAloon

Bulova

et al. 2014

Biol J Linn Soc Lond

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Brain investment is evolutionarily constrained by high costs of neural tissue. Several ecological factors favour the evolution of increased brain investment; we predict reduced brain region investment will accompany the evolution of organismal or social parasitism when parasites rely on host behaviour and cognition to solve ecological problems. To test this idea we investigated whether brain region investments differed between obligate slave‐making Polyergus mexicanus ant workers and their Formica fusca slave workers. Polyergus workers perform little labour for their colonies; enslaved workers of Formica host species forage, excavate nests and tend the brood. We focused on the calyces of the mushroom bodies, central processing brain regions that are larger in social insect workers that perform complex tasks. As predicted we found lower relative investment in mushroom body calyx in P. mexicanus workers than in F. fusca workers; by contrast, enslaved and free F. fusca workers did not differ in mushroom body calyx volume. We then tested whether slave‐makers and hosts differed in brain investment among sensory modalities. Polyergus slave‐makers employ several unique classes of pheromones during raids, and eye size relative to head size was smaller in P. mexicanus workers than in F. fusca workers. The size of antennal brain tissues relative to visual tissues was greater in Polyergus, both in the peripheral sensory lobes and in the mushroom body calyx, suggesting greater relative investment in antennal processing by slave‐makers. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113, 415–422.

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“…This characteristic appears to be widespread, though absent from Rhinolophus bats and cave-dwelling fruit bats [60][61][62]. Molecular evidence based on the presence of a functional short-wave SWS1 opsin gene supports these findings [56].…”

Section: (A) Attraction and Repulsionmentioning

confidence: 78%

Barriers and benefits: implications of artificial night-lighting for the distribution of common bats in Britain and Ireland

Mathews

Roche

Aughney

et al. 2015

Phil. Trans. R. Soc. B

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Artificial lighting is a particular problem for animals active at night. Approximately 69% of mammal species are nocturnal, and one-third of these are bats. Due to their extensive movements—both on a nightly basis to exploit ephemeral food supplies, and during migration between roosts—bats have an unusually high probability of encountering artificial light in the landscape. This paper reviews the impacts of lighting on bats and their prey, exploring the direct and indirect consequences of lighting intensity and spectral composition. In addition, new data from large-scale surveys involving more than 265 000 bat calls at more than 600 locations in two countries are presented, showing that prevalent street-lighting types are not generally linked with increased activity of common and widespread bat species. Such bats, which are important to ecosystem function, are generally considered ‘light-attracted’ and likely to benefit from the insect congregations that form at lights. Leisler's bat ( Nyctalus leisleri ) may be an exception, being more frequent in lit than dark transects. For common pipistrelle bats ( Pipistrellus pipistrellus ), lighting is negatively associated with their distribution on a landscape scale, but there may be local increases in habitats with good tree cover. Research is now needed on the impacts of sky glow and glare for bat navigation, and to explore the implications of lighting for habitat matrix permeability.

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Behavioral evidence for cone-based ultraviolet vision in divergent bat species and implications for its evolution

Cited by 8 publications

References 22 publications

As Blind as a Bat? Opsin Phylogenetics Illuminates the Evolution of Color Vision in Bats

As Blind as a Bat? Opsin Phylogenetics Illuminates the Evolution of Color Vision in Bats

Evidence for adaptive brain tissue reduction in obligate social parasites (Polyergus mexicanus) relative to their hosts (Formica fusca)

Barriers and benefits: implications of artificial night-lighting for the distribution of common bats in Britain and Ireland

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