Abstract
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.
Highlights
The loss of body and eye pigmentation, or albinism, is a convergent feature found in a majority of species adapted to aphotic subterranean habitats, such as caves[1]
These included the following: all 14 species and clades of amphipods (e.g., Fig. 1C) belonging to five genera in three families occupying a variety of subterranean habitats such as the hypotelminorheic, epikarst, cave streams and phreatic aquifers; the palaemonid decapod shrimp Palaemon antrorum; three millipede species in two orders, the cleidogonid Pseudotremia fulgida in the Chordeumatida and two polydesmid Brachydesmus species (Fig. 1B) in the Polydesmida; and an insect, the cixiid planthopper Oliarus polyphemus (Fig. 1A)
These results demonstrated for the first time that a diverse group of albino cave-adapted arthropod species from a variety of subterranean habitats, all showing no cuticular body pigment, retained the ability to synthesize melanin during wound healing, and that phenoloxidase played an important role in this reaction in both albino and non-albino species
Summary
The loss of body and eye pigmentation, or albinism, is a convergent feature found in a majority of species adapted to aphotic subterranean habitats, such as caves[1]. We attempted to determine if cave arthropods lacking body pigmentation have lost the melanization part of the innate immune response. This is not a trivial question because the ability to immediately respond to an immune challenge is critical for survival, maintenance of parts of the innate immunity is costly in terms of resources[7,20]. Subterranean environments are hypothesized to harbor lower abundance and diversity of parasites and pathogens than surface environments (e.g.23), and cave organisms may experience relaxed selection to maintain the highly resource demanding portion of the innate immune system such as the melanin synthesis pathway. We found that the wound melanization response is highly conserved across arthropod taxa, but has been lost in isopods, the chelicerate Limulus polyphemus and the cave shrimp Troglocaris anophthalmus
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