Low but stable frequency of xanthic phenotypes in a population of the twoline pupfish, Cyprinodon bifasciatus.
This communication reports the discovery and temporal persistence of naturally occurring xanthic (yellow) variants of the endangered twoline pupfish Cyprinodon bifasciatus, one of two pupfishes endemic to the Cuatro Cienegas basin, Mexico (Miller, 1968; Carson, 2009a, b). Xanthic phenotypes have been reported in a broad taxonomic array of fishes, including marine [Batrachoididae (Opsanus; Lewis, 1968), Ostraciidae (Lactophrys triqueter; Pattengill-Semmens, 1999) and Sebastidae (Sebastes; Cripe, 1998)] and numerous freshwater representatives [Adrianichthyidae (Oryzias; Goodrich, 1927), Centrachidae (Micropterus; Allen and Neill, 1953), Cichlidae (Cichlasoma and Herichthys; Webber et al., 1973; Konings, 1994), Cyprinodontidae (Cyprinodon; Turner and Liu, 1977), Lepisosteidae, (Lepisosteus; McIlwain and Waller, 1972; Tyler, 1990), Percidae (Etheostoma; Denoncourt et al., 1976) and Poeciliidae (Poecilia (Lebistes); Goodrich et al., 1944; Angus and Blanchard, 1991)]. A simple genetic basis for xanthism potentially explains occurrence across a wide taxonomic profile. For example, in at least one family, Poeciliidae (Cyprinodontiformes) homozygosity of a recessive allele at a single autosomal locus forms the basis of xanthism in several cases, including guppies (Goodrich et al., 1944), swordtails (Gordon, 1957) and sailfin mollies (Angus and Blanchard, 1991).
Despite taxonomic breadth in occurrence, xanthic variants are typically rare within species (Turner and Liu, 1977; Konings, 1994; Pattengill-Semmens, 1999; but see Lewis, 1968). Rarity of xanthic phenotypes is generally assumed to reflect magnified predation risks that attend conspicuity; this supposition is indirectly supported by Endler (1980), who found in both laboratory and field experiments on wild-type guppies that increased conspicuousness is associated with elevated predation risk. However, other factors potentially influence frequency of conspicuous phenotypes within populations. For example, Endler (1980) also showed that sexual selection can favor conspicuousness in low predation environments. Furthermore, in speculating on the sudden appearance and apparent disappearance of xanthic Cyprinodon salinus in Salt Creek, Death Valley National Monument, Turner and Liu (1977) suggested that stochastic processes associated with a fluctuating population might have been important, though a temporary relaxation of natural selection was also proposed. The rarity and unpredictable occurrence of xanthic phenotypes typically precludes the testing of limiting agents in situ. However, the low but stable frequency of such variants in a population of C. bifasciatus provides a system amenable to such empirical investigation.
The isolated, minor spring system of Escobedita (Carson and Dowling, 2006) was visited on four occasions (Jan. 2002, Mar. 2002, Aug. 2002 and Jul. 2003). Visual observations were made within the uniformly clear waters of the three habitat sub-sections: headspring, riachuelo (small creek) and terminal pool-marsh complex. Frequencies of xanthic and wild-type Cyprinodon bifasciatus were estimated after haphazard sampling via seine in Mar. and Aug. 2002. Specimens were collected via seine and dip net within the terminal pool Immediately after capture, a subset of individuals was placed in a homemade viewing apparatus in order to record color characteristics of live fish. Specimens were preserved in 95% ethanol for genetic analysis (Carson and Dowling, 2006) or 10% formalin for morphological study (Tobler and Carson, 2010).
[FIGURE 1 OMITTED]
RESULTS AND DISCUSSION
Xanthic and wild type individuals of Cyprinodon bifasciatus are represented, respectively, in Panels A-B and G-D of Fig. 1, with melanophore distributions highlighted in Panels E and F-G, respectively. Both phenotypes were observed on all four visits (Jan. 2002, Mar. 2002, Aug. 2002 and Jul. 2003) to the terminal pool of Escobedita but not the riachuelo or headspring. Absence from the latter two habitats occurred despite direct connection to the terminal pool (riachuelo) or comparable abundance of C. bifasciatus as was observed in the terminal pool (headspring); however, a natural barrier appears to prevent upstream movement into the headspring habitat. On each visit to the terminal pool, 5-10 individuals of xanthic phenotype, including adults and juveniles, were observed among several hundred wild-type C. bifasciatus. A total of 63 fish were sacrificed over the course of the study, including five xanthic and 58 wild-type individuals. Three xanthic and three wild-type individuals were deliberately captured for preservation in Jan. 2002; the remaining 57 fish were haphazardly captured in Mar. and Aug. 2002, with xanthic individuals accounting for ~3.7% (1/27) and 3.3% (1/30) of the catch, respectively. Sizes of the five captured xanthic individuals ranged from 30.9-40.2 mm SL, though smaller individuals were observed; captured wild-type C. bifasciatus ranged from <20 mm (juvenile) to 47.6 mm (adult male).
Wild-type Cyprinodon bifasciatus color patterns are described in detail
in Miller (1968). Briefly, adult male C. bifasciatus are chalky blue, have yellow eyes and a thin, terminal black band on the caudal fin, whereas females and juveniles have a light blue to pale brown base-color and two prominent dark brown lateral stripes. There is no black band on the caudal fin of females or juveniles; in contrast, lateral stripes are subdued to absent in mature males. All xanthic individuals from Escobedita appeared to resemble the 'golden' and not the 'blond' variant of Poecilia reticulata (Lebistes reticulatus), as described by Goodrich et al. (1944); xanthic C. bifasciatus did not appear similar to the yellow and red phenotypes of Oryzias latipes (Goodrich, 1927) that Turner and Liu (1977) considered to be superficially similar to xanthic C. salinus. Xanthic male and female (or immature male) C. bifasciatus (Panels A and B, respectively) were a base yellow. Lateral stripes were difficult to discern in these individuals, with melanophores in these regions spread more diffusely (Panel E) than in their wild-type counterparts (Panels F and G). In xanthic individuals of both sexes the middle and upper half of the body had regular, triangular concentrations of melanophores over the posterior half of the scales, with the anterior and middle portions of these scales base yellow (Panels A, B and E). Lower portions of the body either lacked melanophores or their presence was more diffuse and slight (Panels A, B and E). The upper, reduced lateral stripe ended in a darkened amorphous to triangular blotch of melanophores at or slightly anterior to the caudal fin base (Panels A and B) and was most pronounced in adult males (Panel A). Xanthic individuals had a soft-white belly and a flash of silver on the cheeks. The lips of mature males exhibited subtle darkening but did not have the purple pigmentation characteristic of wild-type individuals. All fins were pale white to yellow in xanthic fish, with yellow coloration most apparent in the caudal, lower half of the dorsal and pectoral fins. Unlike wild-type males (Panel C), xanthic males (Panel A) exhibited no black terminal band on the caudal fin or black pigmentation on peripheral portions of the pectoral, dorsal and anal fins. Eye color of all xanthic individuals was identical to that in comparable wild-type individuals, including the bright yellow eyes characteristic of mature males; however, in xanthic individuals the tissue around the eyes was translucent rather than opaque, which made the eye-sockets visible.
The low but stable frequency of xanthic Cyprinodon bifasciatus in Escobedita contrasts with expected strong selection against such conspicuous individuals. Thus, regular occurrence of xanthic individuals in this system presents an excellent opportunity to investigate the evolutionary factors that influence the frequency and persistence of these color-phenotypes in natural populations. Three critical questions could be experimentally addressed in the Escobedita population: (1) Does persistence of xanthic C. bifasciatus result from relaxed predation? Unlike most habitats occupied by C. bifasciatus, this system is apparently devoid of large, piscivorous fishes, such as the endemic cichlid Herichthys minckleyi and native centrarchid Micropterus salmoides, normally associated with this species. Furthermore, avian predators are relatively uncommon in the valley, tend to hunt in the more expansive marsh and laguna systems and were never observed at Escobedita on the four visits to this site; (2) Is the relatively high frequency of xanthic C. bifasciatus driven by stochastic processes? It is well established that genetic drift is most pronounced in small populations, and under these circumstances its effects can overwhelm those of even strong natural selection; genetic drift might be especially influential under conditions of relaxed natural selection (e.g., atypically low predation). The population size of C. bifasciatus in Escobedita is small and inbreeding is undoubtedly high. Genetic evidence supports this, as the population is fixed for a single haplotype at the mitochondrial cytochrome b gene (Carson and Dowling, 2006); and (3) Does sexual selection influence the persistence of xanthic C. bifasciatus in Escobedita? It is known that in at least some fishes conspicuous color morphs can be at a selective (reproductive) advantage in low predation environments (Endler, 1980), thus selection could potentially favor xanthic individuals under such circumstances. Sexual selection is an undoubtedly of evolutionary significance in C bifasciatus, as mature males are brightly colored and form breeding leks where territories are defended, females choose mates and copulations are paired (Arnold, 1972). Cyprinodon bifasciatus also hybridize extensively with the phenotypically dissimilar, co-endemic C. atrorus (Carson, 2005; Carson and Dowling, 2006); therefore, sexual selection might at the very least be selectively neutral towards xanthic individuals.
A sparse record exists for xanthic variants in Cyprinodon, with prior observations limited to the Death Valley endemic Salt Creek pupfish, C. salinus, (Turner and Liu, 1977) and R. R. Miller's unpubl, obs. (documented in Turner and Liu, 1977) of xanthic Devils Hole pupfish, C. diabolis, from Ash Meadows National Wildlife Refuge, Nevada. Discovery of xanthic phenotypes of C. bifasciatus extends this record to include a basal member of the genus (Miller, 1968; Echelle et al., 1998) and complements observations of similar color morphs in the endemic Cuatro Cienegas cichlid Herichthys minckleyi (Konings, 1994; D. Hendrickson, pers. comm.). Together, xanthic C. bifasciatus and H. minckleyi add a curious dimension to the highly endemic biota of the Cuatro Cienegas basin, Mexico.
Acknowledgments.--I thank my father, W. E. Carson, as well as S. Minckley and S. Nag, for field assistance. I also am grateful to the Mexican government for providing the collection permit (DOO02-59,853). Funding was awarded through the NASA Astrobiology Initiative, grant number NCC2-1051.
ALLEY, E. R. AND W. T. NEILL. 1953. Xanthic largemouth bass (Micropterus) from Florida. Copeia, 1953:116-117.
ANGUS, R. A. AND P. D. BLANCHARD. 1991. Genetic basis of the gold phenotype in sailfin mollies. J. Hered., 82:425-428.
ARNOLD, E. T. 1972. Behavioral ecology of two pupfishes (Cyprinodontiformes, genus Cyprinodon) from northern Mexico. Ph.D. dissertation, Arizona State University, Tempe.
CARSON, E. W. 2005. Hybridization between Cyprinodon atrorus and C. bifasciatus: history, patterns, and dynamics. Ph.D. dissertation, Arizona State University, Tempe.
--. 2009a. Threatened fishes of the world: Cyprinodon atrorus Miller 1968 (Cyprinodontidae). Environ. Biol. Fish., 86:425-426.
--. 2009b. Threatened fishes of the world: Cyprinodon bifasciatus Miller 1968 (Cyprinodontidae). Environ. Biol. Fish., 86:445-446.
-- AND T. E. DOWLING. 2006. Influence of hydrogeographic history and hybridization on the distribution of genetic variation in the pupfishes Cyprinodon atrorus and C. bifasciatus. Mol. Ecol., 15:667-679.
--, J. J. ELSER AND T. E. DOWLING. 2008. Importance of exogenous selection in a fish hybrid zone: insights from reciprocal transplant experiments. Copeia, 9008:794-800.
CRAVE, D. 1998. Occurrence of xanthic grass rockfish, Sebastes rastrelliger. Calif. Fish Game, 84:100-101.
DENONCOURT, R. F., T. W. ROBBINS AND J. R. STAUFFER. 1976. A description of xanthic tessellated darters, Etheostoma olmstedi (Teleostei: Percidae). Copeia, 1976:813-815.
ENDLER, J. A. 1980. Natural selection on color patterns in Poecilia reticulata. Evolution, 34:76-91. GOODRICH, H. B. 1927. A study of the development of Mendelian characters in Oryzias latipes. J. Exp. Biol., 49:261-287.
--, N. D. JOSEPHSON, J. P. TRINKAUS AND J. M. SLATE. 1944. The cellular expression and genetics of two new genes in Lebistes reticulatus. Genetics, 99:584-592.
GORDON, M. 1957. Physiological genetics of fishes, p. 431-502. In: M. E. Brown (ed.). The physiology of fishes. Academic Press, New York, New York, USA.
KONINGS, A. 1994. An extremely rare colour morph of Herichthys minckleyi, p. 68-69. In: A. Konings (ed.). The cichlids yearbook, Vol. 4. Cichlid Press, St. Leon-Rot, Germany. LEWIS, R. R. 1968. A comparative study of pigmentation of wild and xanthic forms of toadfish, Opsanus beta. Am. Zool., 9:1106.
MCILWAIN, T. D. AND R. WALLER. 1972. A xanthochroic gar, Lepisosteus oculatus, from Mississippi. T. Am. Fish. Soc., 101:362.
MILLER, R. R. 1968. Two new fishes of the genus Cyprinodon from the Cuatro Cienegas basin, Coahuila, Mexico. Occas. Pap. Mus. Zool. U. Mich., 659:1-16.
MINCKLEY, W. L. 1969. Environments of the Bolson of Cuatro Cienegas, Coahuila, Mexico, with Special Reference to the Aquatic Biota. Texas Western Press, El Paso, Texas, USA.
PATTENGILL-SEMMENS, C. V. 1999. Occurrence of a unique color morph in the smooth trunkfish (Lactophrys triqueter L.) at the Flower Garden Banks and Stetson Bank, Northwest Gulf of Mexico. B. Mar. Sci., 65:587-591.
TOBLER, M. AND E. W. CARSON. 2010. Environmental variation, hybridization, and phenotypic diversification of Cuatro Cienegas pupfishes. J. Evolution. Biol., 93:1475-1489.
TURNER, B. J. AND R. K. LIU. 1977. Xanthic variants in a natural population of the Salt Creek pupfish, Cyprinodon salinus. Southwest. Nat., 22:538-540.
TYLER, D. 1990. Xanthochroistic gar in Oklahoma. Southwest. Nat., 35:225.
WEBBER, R., G. W. BARLOW AND A. H. BRUSH. 1973. Pigments of a color polymorphism in a cichlid fish. Comp. Biochem. Physiol., 44:1127-1135.
EVAN W. CARSON (1), Department of Biology, MSC03 2020, One University of New Mexico Way, Albuquerque 87131. Submitted 4 October 2010; Accepted 25 March 2011.
(1) e-mail: firstname.lastname@example.org
|Printer friendly Cite/link Email Feedback|
|Title Annotation:||Notes and Discussion|
|Author:||Carson, Evan W.|
|Publication:||The American Midland Naturalist|
|Date:||Oct 1, 2011|
|Previous Article:||First record of the Silver Lamprey, Ichthyomyzon unicuspis (Petromyzontiformes: Petromyzontidae), from Arkansas.|
|Next Article:||The Whole Tooth and Nothing but the Tooth: A Review of Mammal Teeth: Origin, Evolution, and Diversity.|