Project

The loss of pigmentation in cave animals

Goal: Pigmentation protects animals from solar radiation and has critical roles in temperature control, camouflage, and in species and sex recognition. However, pigmentation is absent in some animals, a condition known as albinism. Albinism is one of the prime examples of convergence in nature because it has evolved repeatedly in phylogenetically distant taxa and in different environments lacking sunlight, regardless of the types of pigments present. Albinism is one of the defining features in animals adapted to cave habitats. Our previous research identified a relevant molecular change in multiple cave animals with melanin pigmentation, and that natural selection as opposed to drift may be involved. However, the exact genes and mutations that control this trait remain elusive. Also, nothing is known about the other pigments that are lost in cave animals.
We will investigate the molecular and evolutionary mechanisms of albinism across different animal groups and the types of pigment they use to understand the mechanisms of cave adaptation at the molecular level (genotype to phenotype) and evolutionary forces related to convergent evolution. We will integrate experimental procedures across biological disciplines (molecular to organismal), using diverse organisms (carefully selected from planarians to vertebrates) from diverse environments (cave and surface, terrestrial and aquatic), and applying various methodological approaches (from laboratory to field).

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Helena Bilandzija
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Selected among 120 applications, cave bivalve Congeria kusceri is running for the "Mollusk of the year". 
The winner will get its genome sequenced, which will be an important milestone in our research. PhD student Magdalena Grgić is working on the loss of pigmentation in cave bivalves.
Help Congeria win the prestigious title by voting at https://tbg.senckenberg.de/mollusc/Magdalena Grgić
 
Helena Bilandzija
added a project goal
Pigmentation protects animals from solar radiation and has critical roles in temperature control, camouflage, and in species and sex recognition. However, pigmentation is absent in some animals, a condition known as albinism. Albinism is one of the prime examples of convergence in nature because it has evolved repeatedly in phylogenetically distant taxa and in different environments lacking sunlight, regardless of the types of pigments present. Albinism is one of the defining features in animals adapted to cave habitats. Our previous research identified a relevant molecular change in multiple cave animals with melanin pigmentation, and that natural selection as opposed to drift may be involved. However, the exact genes and mutations that control this trait remain elusive. Also, nothing is known about the other pigments that are lost in cave animals.
We will investigate the molecular and evolutionary mechanisms of albinism across different animal groups and the types of pigment they use to understand the mechanisms of cave adaptation at the molecular level (genotype to phenotype) and evolutionary forces related to convergent evolution. We will integrate experimental procedures across biological disciplines (molecular to organismal), using diverse organisms (carefully selected from planarians to vertebrates) from diverse environments (cave and surface, terrestrial and aquatic), and applying various methodological approaches (from laboratory to field).
 
Helena Bilandzija
added 4 research items
Many species adapted to aphotic subterranean habitats have lost all body pigmentation. Yet, melanization is an important component of wound healing in arthropods. We amputated appendages in a variety of cave-adapted and surface-dwelling arthropods. A dark clot formed at the site of injury in most species tested, including even albino cave-adapted species. The dark coloration of the clots was due to melanin deposition. The speed of wound melanization was uncorrelated with a difference in metabolic rate between surface and cave populations of an amphipod. The chelicerate Limulus polyphemus, all isopod crustaceans tested, and the cave shrimp Troglocaris anophthalmus did not melanize wounds. The loss of wound melanization in T. anophthalmus was an apomorphy associated with adaptation to subterranean habitats, but in isopods it appeared to be a symplesiomorphy unrelated to colonization of subterranean habitats. We conclude that wound melanization i) is an important part of innate immunity because it was present in all major arthropod lineages, ii) is retained in most albino cave species, and iii) has been lost several times during arthropod evolution, indicating melanization is not an indispensable component of wound healing in arthropods.
Albinism, the reduction or loss of melanin pigment, is found in many diverse cave-dwelling animals. The mechanisms responsible for loss of melanin pigment are poorly understood. In this study we use a melanogenic substrate assay to determine the position where melanin synthesis is blocked in independently evolved cave planthoppers from Hawaii and Croatia. In this assay, substrates of enzymes responsible for melanin biosynthesis are added to fixed specimens in vitro and their ability to rescue black melanin pigmentation is determined. L-tyrosine, the first substrate in the pathway, did not produce melanin pigment, whereas L-DOPA, the second substrate, restored black pigment. Substrates in combination with enzyme inhibitors were used to test the possibility of additional downstream defects in the pathway. The results showed that downstream reactions leading from L-DOPA and dopamine to DOPA-melanin and dopamine-melanin, the two types of insect melanin, are functional. It is concluded that albinism is caused by a defect in the first step of the melanin synthesis pathway in cave-adapted planthoppers from widely separated parts of the world. However, Western blots indicated that tyrosine hydroxylase (TH), the only enzyme shown to operate at the first step in insects, is present in Hawaiian cave planthoppers. Thus, an unknown factor(s) operating at this step may be important in the evolution of planthopper albinism. In the cavefish Astyanax mexicanus, a genetic defect has also been described at the first step of melanin synthesis suggesting convergent evolution of albinism in both cave-adapted insects and teleosts.
Multiple cave populations of the teleost Astyanax mexicanus have repeatedly reduced or lost eye and body pigmentation during adaptation to dark caves. Albinism, the complete absence of melanin pigmentation, is controlled by loss-of-function mutations in the oca2 gene. The mutation is accompanied by an increase in the melanin synthesis precursor L-tyrosine, which is also a precursor for catecholamine synthesis. In this study, we show a relationship between pigmentation loss, enhanced catecholamine synthesis and responsiveness to anaesthesia, determined as a proxy for catecholaminerelated behaviours. We demonstrate that anaesthesia resistance (AR) is enhanced in multiple depigmented and albino cavefish (CF), inversely proportional to the degree of pigmentation loss, controlled by the oca2 gene, and can be modulated by experimental manipulations of L-tyrosine or the catecholamine norepinephrine (NE). Moreover, NE is increased in the brains of multiple albino and depigmented CF relative to surface fish. The results provide new insights into the evolution of pigment modification because NE controls a suite of adaptive behaviours similar to AR that may represent a target of natural selection. Thus, understanding the relationship between loss of pigmentation and AR may provide insight into the role of natural selection in the evolution of albinism via a melanin–catecholamine trade-off. © 2018 The Author(s) Published by the Royal Society. All rights reserved.