Cavefish eye loss in response to an early block in retinal differentiation progression

Stemmer, Manuel; Schuhmacher, Laura; Foulkes, Nicholas S.; Bertolucci, Cristiano; Wittbrodt, Joachim

doi:10.1242/dev.114629

Cited by 40 publications

(36 citation statements)

References 52 publications

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“…In addition, there were fewer signs of apoptosis in the lens tissues. Both findings were in contrast to the known mechanisms underlying eye degeneration in Astyanax cavefish [70]. On the other hand, they found late retinal differentiation events affected and retinal apoptosis to be the driving force of eye degeneration in these fish.…”

Section: Work On Other Cavefish Speciescontrasting

confidence: 71%

Cavefish and the basis for eye loss

Krishnan

Rohner

2017

Phil. Trans. R. Soc. B

110

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One contribution of 17 to a theme issue 'Evo-devo in the genomics era, and the origins of morphological diversity'. Animals have colonized the entire world from rather moderate to the harshest environments, some of these so extreme that only few animals are able to survive. Cave environments present such a challenge and obligate cave animals have adapted to perpetual darkness by evolving a multitude of traits. The most common and most studied cave characteristics are the regression of eyes and the overall reduction in pigmentation. Studying these traits can provide important insights into how evolutionary forces drive convergent and regressive adaptation. The blind Mexican cavefish (Astyanax mexicanus) has emerged as a useful model to study cave evolution owing to the availability of genetic and genomic resources, and the amenability of embryonic development as the different populations remain fertile with each other. In this review, we give an overview of our current knowledge underlying the process of regressive and convergent evolution using eye degeneration in cavefish as an example.This article is part of the themed issue 'Evo-devo in the genomics era, and the origins of morphological diversity'.

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Section: Work On Other Cavefish Speciescontrasting

confidence: 71%

Cavefish and the basis for eye loss

Krishnan

Rohner

2017

Phil. Trans. R. Soc. B

110

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“…However, the peak marker for the PAXB QTL is not included in the CERC QTL interval, suggesting the two chromosome 21 QTL might have distinct genetic bases as well. Thus, it appears that similar changes in morphology (more teeth) have evolved via largely distinct developmental genetic mechanisms, as has been found in sex comb patterning (Tanaka et al, 2009) and wing size (Zwaan et al, 2000) in Drosophila, trunk elongation in salamanders (Parra-Olea and Wake, 2001) and eye loss in different cavefish species (Stemmer et al, 2015).…”

Section: Distinct Genetic Bases Underlie Convergently Evolved Tooth Gainmentioning

confidence: 78%

Distinct developmental and genetic mechanisms underlie convergently evolved tooth gain in sticklebacks

et al. 2015

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Teeth are a classic model system of organogenesis, as repeated and reciprocal epithelial and mesenchymal interactions pattern placode formation and outgrowth. Less is known about the developmental and genetic bases of tooth formation and replacement in polyphyodonts, which are vertebrates with continual tooth replacement. Here, we leverage natural variation in the threespine stickleback fish Gasterosteus aculeatus to investigate the genetic basis of tooth development and replacement. We find that two derived freshwater stickleback populations have both convergently evolved more ventral pharyngeal teeth through heritable genetic changes. In both populations, evolved tooth gain manifests late in development. Using pulse-chase vital dye labeling to mark newly forming teeth in adult fish, we find that both high-toothed freshwater populations have accelerated tooth replacement rates relative to lowtoothed ancestral marine fish. Despite the similar evolved phenotype of more teeth and an accelerated adult replacement rate, the timing of tooth number divergence and the spatial patterns of newly formed adult teeth are different in the two populations, suggesting distinct developmental mechanisms. Using genome-wide linkage mapping in marine-freshwater F2 genetic crosses, we find that the genetic basis of evolved tooth gain in the two freshwater populations is largely distinct. Together, our results support a model whereby increased tooth number and an accelerated tooth replacement rate have evolved convergently in two independently derived freshwater stickleback populations using largely distinct developmental and genetic mechanisms.

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“…The adult fishes completely lack eyes, pigments and scales and their metabolic rate is extremely reduced. In particular, the eye is totally regressed 36 h post fertilization and 1 month later there remains only a rudimentary cyst, with loss of the optic nerves and strongly reduced optic lobes (Berti et al, 2001;Stemmer et al, 2015). This degeneration is rather premature compared, for example, with what is known for the blind Mexican cavefish Astyanax mexicanus.…”

Section: Introductionmentioning

confidence: 96%

Relaxed selective constraints drove functional modifications in peripheral photoreception of the cavefish P. andruzzii and provide insight into the time of cave colonization

et al. 2016

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The genetic basis of phenotypic changes in extreme environments is a key but rather unexplored topic in animal evolution. Here we provide an exemplar case of evolution by relaxed selection in the Somalian cavefish Phreatichthys andruzzii that has evolved in the complete absence of light for at least 2.8 million years. This has resulted in extreme degenerative phenotypes, including complete eye loss and partial degeneration of the circadian clock. We have investigated the molecular evolution of the nonvisual photoreceptor melanopsin opn4m2, whose mutation contributes to the inability of peripheral clocks to respond to light. Our intra-and inter-species analyses suggest that the 'blind' clock in P. andruzzii evolved because of the loss of selective constraints on a trait that was no longer adaptive. Based on this change in selective regime, we estimate that the functional constraint on cavefish opn4m2 was relaxed at ∼ 5.3 Myr. This implies a long subterranean history, about half in complete isolation from the surface. The visual photoreceptor rhodopsin, expressed in the brain and implicated in photophobic behavior, shows similar evolutionary patterns, suggesting that extreme isolation in darkness led to a general weakening of evolutionary constraints on light-responsive mechanisms. Conversely, the same genes are still conserved in Garra barreimiae, a cavefish from Oman, that independently and more recently colonized subterranean waters and evolved troglomorphic traits. Our results contribute substantially to the open debate on the genetic bases of regressive evolution.

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Cavefish eye loss in response to an early block in retinal differentiation progression

Cited by 40 publications

References 52 publications

Cavefish and the basis for eye loss

Cavefish and the basis for eye loss

Distinct developmental and genetic mechanisms underlie convergently evolved tooth gain in sticklebacks

Relaxed selective constraints drove functional modifications in peripheral photoreception of the cavefish P. andruzzii and provide insight into the time of cave colonization

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