Inheritance of a Dominant Spotted Melanic Mutation in the Livebearing Fish Phalloceros caudimaculatus var. reticulata from "Banados del Este" Reserve of Biosphere Site in Uruguay

Abstract

Summary An alternative chromatic variation to the wild-type phenotype of the livebearing fish Phalloceros caudimaculatus (Phalloceros caudimaculatus var. reticulata) was detected in a single female from "Bañados del Este" Reserve of Biosphere Site, in Uruguay. The founder mutant female, which presented a melanic spotted pattern overlapping the wild-type pigmentation, produced laboratory breed strains. Four phenotypes showing different degrees of spotted patterns were obtained. In order to determine the inheritance of this chromatic mutation, experimental crosses and cytogenetic analyses of these laboratory strains were carried out. The breeding experiments among the spotted phenotypic classes and backcrosses suggest the dominant and non-sex linked inheritance of this mutation. Statistical tests demonstrated that the inheritance mechanism of this mutation does not correspond to a 2-gene independent segregation hypothesis as it was proposed in Poecilia sphenops, or to a single dominant gene hypothesis. Additionally, cytogenetic analyses detected a partially heterochromatic biarmed chromosome associated to the inheritance of the pigmentation pattern in laboratory breed strains.

The Biology of Polymorphic Melanic Side-Spotting Patterns in Poeciliid Fishes

“…Unspotted morphs are born without spots and remain unspotted for their entire life (Schröder, 1964;Angus, 1983). In the wild, poeciliids are born unspotted; spots often appear as secondary sexual characteristics begin to develop, such as the gonopodium in immature males, but the melanic side-spotting pattern is not fully established until after the fish is sexually mature, after which it can increase with age in some species (Bellamy, 1924(Bellamy, , 1928Myers, 1925;Gordon, 1931b;Regan, 1961;Atz, 1962;Kallman and Atz, 1966;Kallman, 1971;Menzel and Darnell, 1973;Angus, 1983;Martin, 1984;Franck et al, 1998;Angus et al, 1999;Meyer et al, 2006;Gutiérrez and García, 2007). For some spotted or all-black laboratory strains, spotted morphs can be born unspotted or spotted and either develop into spotted or completely black morphs after sexual maturity (Schröder, 1964;Angus, 1983).…”

“…When present, the frequency of spotted individuals varies depending on the population and species. In wild populations within their native range, spotted patterns ranged from a frequency of <0.5 to 28% of individuals in Xiphophorus maculatus, X. helleri, X. variatus, X. cortezi, G. holbrooki, Phalloceros caudimaculatus, and Poecilia mexicana (Gordon, 1943(Gordon, , 1948Gordon and Gordon, 1957;Regan, 1961;Kallman, 1971;Snelson et al, 1986;Karplus and Algom, 1996;Horth, 2004;Gutiérrez and García, 2007;Culumber et al, 2014). Rarely, extreme populations occur with higher frequencies of spotted morphs ranging from 40 to over 70%, as seen in X. cortezi, X. variatus, and X.…”

“…Melanic side-spotting patterns likely arose through random, spontaneous mutations in the pigmentation pathway. Spontaneous mutations can maintain novel phenotypes at low frequencies within populations if the mutations occur at a similar or higher rate than they are selected out of a population (Gordon and Gordon, 1957;Angus, 1983;Horth, 2006;Gutiérrez and García, 2007); however, spontaneous mutation rates are very low, and the frequencies seen in most poeciliid populations would require an improbably high mutation rate, suggesting the wide taxonomic distribution and persistence of poeciliid side-spotting is instead maintained by other processes (Huxley, 1955;Horth, 2006;Gray and McKinnon, 2007;Forsman et al, 2008;McKinnon and Pierotti, 2010). Furthermore, melanic side-spotting patterns appear to be evolutionarily stable, as macromelanophore-based patterns have possibly existed within poeciliid species for millions of years (Kazianis and Borowsky, 1995).…”

“…The melanic side-spotting pattern is always a genetically dominant trait (Gordon, 1927(Gordon, , 1937Fraser and Gordon, 1929;Gordon and Smith, 1938;Gordon and Gordon, 1957;Atz, 1962;Schröder, 1964;Zander, 1965;Kallman and Atz, 1966;Kallman, 1971;Angus, 1983Angus, , 1989Horth, 2006;Gutiérrez and García, 2007). Long-term persistence of a dominant trait indicates that multiple positive and negative selective pressures likely act upon the pattern and its correlated traits (Gordon and Gordon, 1957).…”

“…Direction of effect is listed as increased (+), decreased (−), and no difference (/) for the spotted morph compared to the unspotted morph. Gordon, 1931a;Regan, 1961;Vielkind, 1976;Anders et al, 1984;Kottler et al, 2020 Skin regeneration and grafts , 1924Myers, 1925;Gordon, 1931b;Schröder, 1964;Angus, 1983;Martin, 1984;Gutiérrez and García, 2007 Male expression > female expression…”