Selection and the Maintenance of a Colour Pattern Polymorphism in the Green Swordtail (Xiphophorus Helleri)

Abstract

Many Xiphophorus populations include a number of individuals with black spots on body sides or fins. In many cases such spots are composed of extremely large melanophore cells, the so-called macromelanophores. Macromelanophore pattern polymorphism is known in 10 out of 22 Xiphophorus species. In at least 8 species alleles of the macromelanophore determining locus Mdl are intimately linked to a dominant oncogene, ONC-Xmrk, which can give rise to malignant skin tumors (melanoma). We present, for the first time, evidence that macromelanophore pattern polymorphisms may be maintained by selection in a seasonally variable environment. In school-choice experiments single Xiphophorus helleri females spent more time with groups of spotted females than with non-spotted females under turbid, but not under clear water conditions. Similarly, receptive females preferred spotted males in turbid, but not in clear water. Thus, in nature, when the water becomes turbid after heavy rainfalls, school mates and reproductive partners can evidently find each other more easily with the help of macromelanophore spotting patterns. Intrasexual selection seems to be irrelevant because spotted and non-spotted males were equally successful in competition experiments. A genetic hitchhiking scenario is discussed which could explain the fact that the potentially injurious tumor gene ONC-Xmrk has been maintained in the genus Xiphophorus over a period of millions of years by its close linkage to positively selected macromelanophore alleles.

Evolution of Xmrk: an oncogene, but also a speciation gene?

“…One such function could be that the Mdl encoded pigment spots facilitate the finding of conspecific individuals for shoaling behavior, in particular when the turbidity of the water is high. (57,58) This situation is quite common in the majority of habitats, after each heavy rainfall. On the other hand, such spots may make the fish more conspicuous to predators in clear water creating a disadvantage.…”

Melanin pattern morphs do not differ in metabolic rate: implications for the evolutionary maintenance of a melanophore polymorphism in the green swordtail, Xiphophorus helleri

“…Female Xiphophorus helleri appear to detect spotted conspecifics more easily than nonspotted conspecifics in cloudy (but not in clear) water and the polymorphism may be maintained by selection in a seasonally variable environment (Franck et al 2001).…”

Mate choice for more melanin as a mechanism to maintain a functional oncogene

“…Remarkably, Xmrk has become more efficient since its origin, incorporating two gain-of-function mutations within its coding region that lead to ligandindependent dimerization (12). Because Xmrk is always correlated with specific macromelanophore patterns (13,15), these patterns have been suggested to play a key role in maintaining Xmrk (12,34). Despite this, we are aware of only one other study that has detected selection for a macromelanophore pattern (34), and this study was conducted on Xiphophorus helleri, which lacks the Xmrk genotype (15).…”

“…Because Xmrk is always correlated with specific macromelanophore patterns (13,15), these patterns have been suggested to play a key role in maintaining Xmrk (12,34). Despite this, we are aware of only one other study that has detected selection for a macromelanophore pattern (34), and this study was conducted on Xiphophorus helleri, which lacks the Xmrk genotype (15). It is intriguing that both patterns, dabbed (X. helleri) (35) and spotted (X. coretzi) (16) caudal, are determined by autosomal genes and are not sex-linked.…”