Expanded expression of Sonic Hedgehog in<i>Astyanax</i>cavefish:multiple consequences on forebrain development and evolution

Menuet, Arnaud; Alunni, Alessandro; Joly, Jean‐Stéphane; Jeffery, William R.; Rétaux, Sylvie

doi:10.1242/dev.02780

Cited by 112 publications

(144 citation statements)

References 80 publications

(89 reference statements)

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“…Such comparisons are difficult to make in mammals, because deep evolutionary distances separate lineages and considerable size variation obscures brain adaptations (11,16,30). Our conclusion extends those from studies of cavefishes and birds (31,32), and suggests that evolution might capture any point along the continuum of patterning and neurogenesis as neural systems diversify.…”

Section: Manipulation Of Wnt Signaling Mimics Natural Variation Amongsupporting

confidence: 52%

Brain diversity evolves via differences in patterning

Sylvester

Rich

Loh

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

122

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Differences in brain region size among species are thought to arise late in development via adaptive control over neurogenesis, as cells of previously patterned compartments proliferate, die, and/or differentiate into neurons. Here we investigate comparative brain development in ecologically distinct cichlid fishes from Lake Malawi and demonstrate that brains vary among recently evolved lineages because of early patterning. Divergence among rock-dwellers and sand-dwellers in the relative size of the telencephalon versus the thalamus is correlated with gene expression variation in a regulatory circuit (composed of six3, fezf2, shh, irx1b, and wnt1) known from model organisms to specify anterior-posterior (AP) brain polarity and position the shh-positive signaling boundary zona limitans intrathalamica (ZLI) in the forebrain. To confirm that changes in this coexpression network are sufficient to produce the differences we observe, we manipulated WNT signaling in vivo by treating rockdwelling cichlid embryos with temporally precise doses of LiCl. Chemically treated rock-dwellers develop gene expression patterns, ZLIs, and forebrains distinct from controls and untreated conspecifics, but strongly resembling those of sand-dwellers. Notably, endemic Malawi rock-and sand-dwelling lineages are alternately fixed for an SNP in irx1b, a mediator of WNT signaling required for proper thalamus and ZLI. Together, these natural experiments in neuroanatomy, development, and genomics suggest that evolutionary changes in AP patterning establish ecologically relevant differences in the elaboration of cichlid forebrain compartments. In general, variation in developmental patterning might lay the foundations on which neurogenesis erects diverse brain architectures.A rguably the most-studied vertebrate organ, the brain has played an important role in the evolution of our own species. Modifications of brain structure are responsible for novel behaviors that galvanized evolutionary radiation of the major vertebrate groups (1). Following decades of research in model organisms, we now know a great deal about how the process of development makes a brain (2). We know much less about evolutionary mechanisms of brain diversification. The brain develops under the iterative influence of antagonistic anterior and posterior signaling molecules, inductive and repressive transcription factors that receive those signals, and lineage restriction boundaries that define compartments (2, 3). Just after gastrulation, the initial anterior-posterior (AP) polarity of the brain is established by a tug-of-war between posteriorizing signals (e.g., wnt1) secreted from the midbrain-hindbrain boundary (MHB) and WNT antagonists (e.g., six3, tlc) expressed from the anterior neural ridge (ANR). The MHB develops to demarcate the hindbrain from the fore-plus midbrain (Fig. S1). With the subsequent formation of the diencephalon-midbrain boundary and the zona limitans intrathalamica (ZLI), the forebrain and midbrain begin to follow separate paths of development.These ini...

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Section: Manipulation Of Wnt Signaling Mimics Natural Variation Amongsupporting

confidence: 52%

Brain diversity evolves via differences in patterning

Sylvester

Rich

Loh

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

122

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“…Alternatively, this result could be an artifact of lab rearing. For example, the large adults may have learned that they can better acquire food by responding to olfactory (Menuet et al, 2007) or auditory cues, rather than oscillatory flow when fed in aquaria. Large Pachón cavefish also showed no VAB (Fig.…”

Section: Io-3 Eomentioning

confidence: 99%

The sensitivity of lateral line receptors and their role in the behavior of Mexican blind cavefish (Astyanax mexicanus)

Yoshizawa

Jeffery

Netten

et al. 2013

Journal of Experimental Biology

124

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The characid fish species Astyanax mexicanus offers a classic comparative model for the evolution of sensory systems. Populations of this species evolved in caves and became blind while others remained in streams (i.e. surface fish) and retained a functional visual system. The flow-sensitive lateral line receptors, called superficial neuromasts, are more numerous in cavefish than in surface fish, but it is unclear whether individual neuromasts differ in sensitivity between these populations. The aims of this study were to determine whether the neuromasts in cavefish impart enhanced sensitivity relative to surface fish and to test whether this aids their ability to sense flow in the absence of visual input. Sensitivity was assessed by modeling the mechanics and hydrodynamics of a flow stimulus. This model required that we measure the dimensions of the transparent cupula of a neuromast, which was visualized with fluorescent microspheres. We found that neuromasts within the eye orbit and in the suborbital region were larger and consequently about twice as sensitive in small adult cavefish as in surface fish. Behavioral experiments found that these cavefish, but not surface fish, were attracted to a 35 Hz flow stimulus. These results support the hypothesis that the large superficial neuromasts of small cavefish aid in flow sensing. We conclude that the morphology of the lateral line could have evolved in cavefish to permit foraging in a cave environment.

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“…The anterior expression domain of the morphogen sonic hedgehog (Shh) at the embryonic ventral midline is expanded throughout cavefish forebrain development (Menuet et al, 2007;Yamamoto et al, 2004). The secondary loss of eyes is the most spectacular indirect consequence of this increased Shh signalling (Yamamoto et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

“…However, expanded Shh also causes significant and specific modifications in the ventral telencephalon and hypothalamus. In fact, Shh-dependent variations in proliferative activity and in expression of Nkx and LIMhomeodomain transcription factors induce variations in specification and migrations of specific neuronal populations (Menuet et al, 2007). Besides these specific changes, the global early patterning of the forebrain, including the retina, is normal in cavefish.…”

Section: Introductionmentioning

confidence: 99%

“…Indeed, the cavefish eyes undergo normal morphogenesis, growth and patterning during the first 24 hours of development, except for a slightly smaller retina size and a reduced or absent ventral quadrant of the retina, a hallmark of the cavefish embryonic eye (Alunni et al, 2007;Yamamoto and Jeffery, 2000;Yamamoto and Jeffery, 2002). The degeneration and loss of eyes in cavefish occur later and progressively in the following days and weeks (Alunni et al, 2007;Jeffery, 2001;Jeffery, 2005;Wilkens, 2007), and are triggered by lens apoptosis which starts after the first day of development (Strickler et al, 2007;Yamamoto and Jeffery, 2000). Thus, the marked increase in midline Shh expression in cavefish embryos does not have the deleterious consequences one might expect for such a powerful morphogen (for a review, see Monuki, 2007).…”

Section: Introductionmentioning

confidence: 99%

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Restoring eye size in Astyanax mexicanus blind cavefish embryos through modulation of the Shh and Fgf8 forebrain organising centres

Pottin¹,

Hinaux²,

Rétaux³

2011

Development

131

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SUMMARYThe cavefish morph of the Mexican tetra (Astyanax mexicanus) is blind at adult stage, although an eye that includes a retina and a lens develops during embryogenesis. There are, however, two major defects in cavefish eye development. One is lens apoptosis, a phenomenon that is indirectly linked to the expansion of ventral midline sonic hedgehog (Shh) expression during gastrulation and that induces eye degeneration. The other is the lack of the ventral quadrant of the retina. Here, we show that such ventralisation is not extended to the entire forebrain because fibroblast growth factor 8 (Fgf8), which is expressed in the forebrain rostral signalling centre, is activated 2 hours earlier in cavefish embryos than in their surface fish counterparts, in response to stronger Shh signalling in cavefish. We also show that neural plate patterning and morphogenesis are modified in cavefish, as assessed by Lhx2 and Lhx9 expression. Inhibition of Fgf receptor signalling in cavefish with SU5402 during gastrulation/early neurulation mimics the typical surface fish phenotype for both Shh and Lhx2/9 gene expression. Fate-mapping experiments show that posterior medial cells of the anterior neural plate, which lack Lhx2 expression in cavefish, contribute to the ventral quadrant of the retina in surface fish, whereas they contribute to the hypothalamus in cavefish. Furthermore, when Lhx2 expression is rescued in cavefish after SU5402 treatment, the ventral quadrant of the retina is also rescued. We propose that increased Shh signalling in cavefish causes earlier Fgf8 expression, a crucial heterochrony that is responsible for Lhx2 expression and retina morphogenesis defect.

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Expanded expression of Sonic Hedgehog inAstyanaxcavefish:multiple consequences on forebrain development and evolution

Cited by 112 publications

References 80 publications

Brain diversity evolves via differences in patterning

Brain diversity evolves via differences in patterning

The sensitivity of lateral line receptors and their role in the behavior of Mexican blind cavefish (Astyanax mexicanus)

Restoring eye size in Astyanax mexicanus blind cavefish embryos through modulation of the Shh and Fgf8 forebrain organising centres

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