Genotyping-by-sequencing supports a genetic basis for alpine wing-reduction in a New Zealand stonefly

Aj, Veale; Bj, Foster; Pk, Dearden; Jm, Waters

doi:10.1101/264473

Cited by 4 publications

(6 citation statements)

References 96 publications

(84 reference statements)

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“…We agree that genome-wide approaches provide the best evidence for informing all types of biological research, but also note that selection at one or a few loci can generate the illusion of taxonomic diversity (e.g. Veale et al 2018). For instance, there are several cases in which populations previously recognised by avian systematists as distinct (e.g.…”

supporting

confidence: 52%

The importance of recognising and conserving biological diversity: a reply to Dussex et al. (2018)

Rawlence¹,

Waters²

2018

NZ J Ecol

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supporting

confidence: 52%

The importance of recognising and conserving biological diversity: a reply to Dussex et al. (2018)

Rawlence¹,

Waters²

2018

NZ J Ecol

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“…The short-winged phenotype is considered to be an adaptive response to the severe environmental conditions of alpine zones: cold temperature, strong winds, and strong ultraviolet radiation (Byers, 1969;Dussex, Chuah, & Waters, 2016;Hodkinson, 2005), and it has been reported in various taxa of insects (Carpenter, 1953;Dussex et al, 2016;Emerson & Wallis, 1995;McCulloch, Wallis, & Waters, 2009;McCulloch & Waters, 2017;Veale, Foster, Dearden, & Waters, 2018;Wallis & Trewick, 2009). Panorpodes paradoxus (Mecoptera, Panorpodidae; Figure 1), which is distributed within the Japanese Archipelago, is known for exhibiting two phenotypes within one species.…”

mentioning

confidence: 99%

Parallel evolution of an alpine type ecomorph in a scorpionfly: Independent adaptation to high‐altitude environments in multiple mountain locations

Suzuki

Tojo

2019

Molecular Ecology

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Elucidation of the diversification process of organisms is one of the important tasks of biology. From the viewpoint of species diversity, insects are the most successful group among the diverse organisms on earth and evolutionary adaptation is one of the important factors driving this pattern. Evolutionary adaptation is one of the important factors in the diversification of insects. One of the representative examples of environmental adaptation in insects is the shortening and loss of wings in subalpine and alpine zones. In this study, we focused on the Japanese scorpionfly, Panorpodes paradoxus. In this species, individuals that inhabit mountainous regions and subalpine zones have long wings (the “general type”), and individuals that inhabit higher altitudinal ranges have short wings (the “alpine type”). We collected samples of all Japanese Panorpodes species and one Korean Panorpodes species, and conducted molecular phylogenetic analyses of the mtDNA COI (610 bp), COII (688 bp), and 16S rRNA (888 bp) and nuDNA EF1‐α (658 bp) and 28S rRNA (524 bp) regions in order to reveal the evolutionary history of the alpine type of P. paradoxus. As a result of molecular phylogenetic analyses, it was revealed that the alpine type of P. paradoxus was polyphyletic, and had evolved to become the alpine type at least twice independently at separate mountain locations. In addition, the result of divergence time estimation suggested that the alpine type is an “ecomorph”, having recently adapted to low temperature habitats following mountain uplift within the Japanese Archipelago and subsequent glacial‐interglacial cycles.

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“…Given that these sympatric full-winged and wing-reduced ecotypes have similar genetic backgrounds (4, 38), our study provides direct evidence for secondary degradation of olfactory acuity associated with flight loss, while eliminating potentially confounding ecological and evolutionary factors that might also affect olfactory processing.…”

Section: Resultsmentioning

confidence: 81%

Adaptive evolution of olfactory degeneration in recently flightless insects

Neupert

McCulloch

Foster

et al. 2020

Preprint

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12Fast-moving animals need fast-acting sensory systems. Flying insects have thus evolved exceptionally 13 quick visual (1) and olfactory processing ability (2). For example, flighted insects can track the temporal 14 structure of turbulent odor plumes at rates above 100 Hz (3). The evolutionary lability of such sensory 15 systems, however, remains unknown. We test for rapid evolutionary shifts in olfactory processing speed 16 associated with flight loss, through neurobiological comparisons of sympatric flighted versus flightless 17 lineages within a wing-polymorphic stonefly species. Our analyses of sensory responses reveal that 18 recently-evolved flightless lineages have substantially degraded olfactory acuity. By comparing flighted 19 versus flightless ecotypes with similar genetic backgrounds (4), we eliminate other confounding factors 20 that might have affected the evolution of their olfactory reception mechanisms. Our detection of 21 different patterns of degraded olfactory sensitivity and speed in independently wing-reduced lineages 22highlights parallel evolution of sensory degeneration. These reductions in sensory ability also echo the 23 rapid vestigialization of wings themselves (4, 5), and represent a neurobiological parallel to the 24 convergent phenotypic shifts seen under sharp selective gradients in other systems (e.g. parallel loss of 25 vision in diverse cave fauna (6)). Our study provides the first direct evidence for the hypothesis that 26flight poses a selective pressure on the speed of olfactory receptor neurons. Our findings also emphasize 27 the energetic costs of rapid olfaction, and the key role of natural selection in shaping dramatic 28 neurobiological shifts. 29 30 31Significance Statement 32Flying insects move fast and have therefore evolved exceptionally quick-acting sensory systems. The 33speed with which such neurobiological shifts can evolve, however, remains unclear. Under the 'use it 34 or lose it' hypothesis, loss of flight should lead to degradation of this fast sensory processing ability. 35 We test for evolutionary reductions in olfactory acuity linked to flight loss, through neurobiological 36 comparisons of flightless versus flighted lineages within a wing-polymorphic insect. Our analyses 37 reveal that newly wing-reduced populations have substantially degraded olfactory acuity, with parallel 38 reductions in this sensory ability detected in independently flightless lineages. These findings reveal 39 that flight poses strong selective pressure for rapid olfaction, and highlight the potential of natural 40 selection in rapidly shaping adaptive shifts in animal sensory systems. 41 42The origin of flight posed novel challenges for animals' sensory systems, including the need for rapid 43 processing of environmental information. Major sensory shifts were needed to compensate for the fact 44 that flying animals move faster and therefore experience more rapid changes in sensory stimuli (vision: 45 (7, 8); olfaction: (2)). This need for rapid sensing seems to be particularly ...

show abstract

Genotyping-by-sequencing supports a genetic basis for alpine wing-reduction in a New Zealand stonefly

Cited by 4 publications

References 96 publications

The importance of recognising and conserving biological diversity: a reply to Dussex et al. (2018)

The importance of recognising and conserving biological diversity: a reply to Dussex et al. (2018)

Parallel evolution of an alpine type ecomorph in a scorpionfly: Independent adaptation to high‐altitude environments in multiple mountain locations

Adaptive evolution of olfactory degeneration in recently flightless insects

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