Morphological colour adaptation during development in fish: involvement of growth hormone receptor 1

ABSTRACTMorphological background adaptation is both an endocrine and a nervous response, involving changes in the amount of chromatophores and pigment concentration. However, whether this adaptation takes place at early developmental stages is largely unknown. Somatolactin (Sl) is a pituitary hormone present in fish, which has been associated to skin pigmentation. Moreover, growth hormone receptor type 1 (Ghr1) has been suggested to be the Sl receptor and was associated with background adaptation in adults. In this context, the aim of this work was to evaluate the ontogeny of morphological adaptation to background and the participation of ghr1 in this process. We found in larval stages of the cichlid Cichlasoma dimerus that the number of head melanophores and pituitary cells immunoreactive to Sl was increased in individuals reared with black backgrounds compared with that in fish grown in white tanks. In larval stages of the medaka Oryzias latipes, a similar response was observed, which was altered by ghr1 biallelic mutations using CRISPR/Cas9. Interestingly, melanophore and leucophore numbers were highly associated. Furthermore, we found that somatic growth was reduced in ghr1 biallelic mutant O. latipes, establishing the dual function of this growth hormone receptor. Taken together, these results show that morphological background adaptation is present at early stages during development and that is dependent upon ghr1 during this period.

Genetic deciphering of the antagonistic activities of the melanin-concentrating hormone and melanocortin pathways in skin pigmentation

The genetic origin of human skin pigmentation remains an open question in biology. Several skin disorders and diseases originate from mutations in conserved pigmentation genes, including albinism, vitiligo, and melanoma. Teleosts possess the capacity to modify their pigmentation to adapt to their environmental background to avoid predators. This background adaptation occurs through melanosome aggregation (white background) or dispersion (black background) in melanocytes. These mechanisms are largely regulated by melanin-concentrating hormone (MCH) and α-melanocyte–stimulating hormone (α-MSH), two hypothalamic neuropeptides also involved in mammalian skin pigmentation. Despite evidence that the exogenous application of MCH peptides induces melanosome aggregation, it is not known if the MCH system is physiologically responsible for background adaptation. In zebrafish, we identify that MCH neurons target the pituitary gland-blood vessel portal and that endogenous MCH peptide expression regulates melanin concentration for background adaptation. We demonstrate that this effect is mediated by MCH receptor 2 (Mchr2) but not Mchr1a/b. mchr2 knock-out fish cannot adapt to a white background, providing the first genetic demonstration that MCH signaling is physiologically required to control skin pigmentation. mchr2 phenotype can be rescued in adult fish by knocking-out pomc, the gene coding for the precursor of α-MSH, demonstrating the relevance of the antagonistic activity between MCH and α-MSH in the control of melanosome organization. Interestingly, MCH receptor is also expressed in human melanocytes, thus a similar antagonistic activity regulating skin pigmentation may be conserved during evolution, and the dysregulation of these pathways is significant to our understanding of human skin disorders and cancers.

Morphological colour adaptation during development: Involvement of Growth Hormone Receptor 1

Morphological background adaptation is both an endocrine and a nervous response, involving changes in the amount and shape of chromatophores. However, if this adaptation takes place at early developmental stages is largely unknown. Somatolactin (SL) is a pituitary hormone present in fish, which has been associated to skin pigmentation. Moreover, growth hormone receptor type 1 (ghr1) has been suggested to be the SL receptor and was associated to background adaptation in adults. In this context, the aim of this work was to evaluate the ontogeny of morphological adaptation to background and the participation of ghr1 in this process. We found in larval stages of Cichlasoma dimerus that the number of head melanophores and ir-SL pituitary cells were increased in individuals reared in black backgrounds compared to fish grown in white tanks. In medaka (Oryzias latipes) larval stages a similar response was observed that is altered by a ghr1 biallelic mutations using CRISPR/cas9. Interestingly, melanophore and leucophore numbers are highly associated. Furthermore, we found that somatic growth is reduced in ghr1 biallelic mutant medaka, establishing the dual function of this growth hormone receptor. Taken together, these results show that morphological background adaptation is present at early stages during development and that is dependent upon ghr1 unless during this period.

Colour vision and background adaptation in a passerine bird, the zebra finch ( Taeniopygia guttata )

Today, there is good knowledge of the physiological basis of bird colour vision and how mathematical models can be used to predict visual thresholds. However, we still know only little about how colour vision changes between different viewing conditions. This limits the understanding of how colour signalling is configured in habitats where the light of the illumination and the background may shift dramatically. I examined how colour discrimination in zebra finch ( Taeniopygia guttata ) is affected by adaptation to different backgrounds. I trained finches in a two-alternative choice task, to choose between red discs displayed on backgrounds with different colours. I found that discrimination thresholds correlate with stimulus contrast to the background. Thresholds are low, and in agreement with model predictions, for a background with a red colour similar to the discs. For the most contrasting green background, thresholds are about five times higher than this. Subsequently, I trained the finches for the detection of single discs on a grey background. Detection thresholds are about 2.5 to 3 times higher than discrimination thresholds. This study demonstrates close similarities in human and bird colour vision, and the quantitative data offer a new possibility to account for shifting viewing conditions in colour vision models.

Unexpectedly low UV-sensitivity in a bird, the budgerigar

Photoreceptor adaptation ensures appropriate visual responses during changing light conditions and contributes to colour constancy. We used behavioural tests to compare UV-sensitivity of budgerigars after adaptation to UV-rich and UV-poor backgrounds. In the latter case, we found lower UV-sensitivity than expected, which could be the result of photon-shot noise corrupting cone signal robustness or nonlinear background adaptation. We suggest that nonlinear adaptation may be necessary for allowing cones to discriminate UV-rich signals, such as bird plumage colours, against UV-poor natural backgrounds.