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Mitochondrial DNA Variation in Pupfishes Assigned to the Species

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Mitochondrial DNA Variation in Pupfishes Assigned to the Species Mitochondrial DNA Variation in Pupfishes Assigned to the Species Cyprinodon macularius (Atherinomorpha: Cyprinodontidae): Taxonomic Implications and Conservation Genetics Author(s): Anthony A. Echelle, Ronald A. van den Bussche, Terrence P. Malloy, Jr., Michelle L. Haynie and C. O. Minckley Source: Copeia, Vol. 2000, No. 2 (May 8, 2000), pp. 353-364 Published by: American Society of Ichthyologists and Herpetologists (ASIH) Stable URL: http://www.jstor.org/stable/1448183 . Accessed: 22/07/2014 12:05 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. American Society of Ichthyologists and Herpetologists (ASIH) is collaborating with JSTOR to digitize, preserve and extend access to Copeia. http://www.jstor.org This content downloaded from 128.123.44.23 on Tue, 22 Jul 2014 12:05:11 PM All use subject to JSTOR Terms and Conditions Copeia,2000(2), pp. 353-364 Mitochondrial DNA Variation in Pupfishes Assigned to the Species Cyprinodonmacularius (Atherinomorpha: Cyprinodontidae): Taxonomic Implications and Conservation Genetics ANTHONY A. ECHELLE, RONALD A. VAN DEN BUSSCHE, TERRENCE P. MALLOYJR., MICHELLE L. HAYNIE, AND C. O. MINCKLEY Variationin mitochondrialDNA (mtDNA)was assessed in a captive stock and 11 wild populations (n = 259) from throughout the native range of Desert Pupfish Cyprinodonmacularius as traditionallyunderstood. Using PCR-SSCP,18 composite haplotypes were identified from a 333-bpsegment of the mitochondrialD-loop and two segments of the ND2 gene (333 and 325 bp). Representativesof each haplotype were sequenced for the entire ND2 gene and the 337-bp segment of the D-loop. Phylogeneticanalyses revealed that haplotypes form two monophyleticgroups, one in the Rio Sonoyta/QuitobaquitoSprings area and one in the Salton Sea/Colorado River Delta. This, with previous observations on morphology, color pattern, and geological history, supports recognition of the Rio Sonoyta/Quitobaquitopopula- tions as a separate species, the QuitobaquitoPupfish C. eremusMiller and Fuiman, from the more widespread desert pupfish C. maculariusBaird and Girard. More than 70% of mtDNA diversityacross all populationswas attributableto differences between the two species. Withinspecies, the averagelocal population contains94% and 97% of the diversityin, respectively,C. eremusand C. macularius.Differences between the Salton Sea and Colorado River Delta populations of C. maculariusex- plain a small (3.7%), but statisticallysignificant, portion of mtDNA diversityin this species. This and the history of connections between Salton Sea and the delta sug- gest that the two regions should be managed separately with no intermixing of pupfish other than what occurs when the present, human-regulatedhydrology is overcome by natural flooding. Haplotype frequencies in C. eremusfrom Quitoba- quito Springsand Rio Sonoytawere not significantlydifferent. However,the poten- tially long history of isolation between these two populationsand evidence of some degree of morphologicaldivergence indicate a need for conservativemanagement with no intermixing.The captive stock exhibited reduced mtDNAvariation relative to its wild parent population from a locality on the delta. Variaci6nde ADNmt fue examinado por una cepa de cautivo y 11 poblaciones silvestres (n = 259) de todas partes del rango natural del cachorrito del desierto Cyprinodonmacularius como entendido tradicionalmente.Utilizando PCR-SSCP,18 haplotipos compuestos fueron identificados desde un segmento de 337-pb del D- loop mitocondrialy dos segmentos del gene DN2 (333 pb y 325 pb). Representantes de cada haplotipo fueron sequenciados por el gene DN2 entero y el segmento de 337-pb del D-loop. Anilisis filogenetico mostr6 una relaci6n monofileticareciproca entre poblaciones de dos regiones generales, Rio Sonoyta/Quitobaquitoy Salton Sea/Delta del Rio Colorado. Esto, con observacionesprevias de morfologia,patr6n de color, y la hist6ria geol6gica, sostiene el reconocimiento de las poblaciones de Rio Sonoyta/Quitobaquitocomo una especie distinta,el cachorritode Quitobaquito C. eremus Miller and Fuiman, de la especie con una distribuci6nmis amplia, el cachorritodel desierto C. maculariusBaird and Girard.Mis de 70%de la diversidad ADNmt de todas las poblaciones fue atribuidaa diferencias entre las dos especies. Dentro de cada especie, la poblaci6n promedia local contiene 94% y 97% de la diversidadde, respectivamente,C. eremusy C. macularius.Las diferencias entre las poblaciones de C. maculariusdel Salton Sea y las de la Delta del Rio Colorado explican una pequefia (3.7%) pero una porci6n estadisticamentesignificativa de la diversidadADNmt de esta especie. Esto y la historia de conecciones entre el Salton Sea y la delta sugieren que los dos regiones deben ser manejadasaparte sin mezclar a los cachorritosmis que lo que ya ocurre cuando la hidrologia actual controlada por los humanos, esti conquistadapor inundacionesnaturales. Frequencias de los haplotipos en C. eremusdel Quitobaquito Springs y el Rio Sonoyta no fueron sig- O2000 by the American Society of Ichthyologists and Herpetologists This content downloaded from 128.123.44.23 on Tue, 22 Jul 2014 12:05:11 PM All use subject to JSTOR Terms and Conditions 354 COPEIA, 2000, NO. 2 nificativamentediferentes. No obstante, la historia probablementelarga del aisla- miento de estas dos poblaciones y la evidencia de alg6n grado de divergenciamor- fol6gica indican la necesidad de un manejo conservativosin mezclarlas formas. La cepa a cautivamostr6 variaci6nreducida de ADNmt en relaci6n a la de su poblaci6n silvestre de origin de una localidad en la delta. Desert Pupfish Cyprinodonmacularius is aimed primarily at resolving evolutionary rela- THElisted as an endangered species by the In- tionships among western pupfishes and includ- ternational Union for Conservation of Nature ed samples from only one or two localities and Natural Resources (Miller, 1979) and by the (Turner, 1974; Echelle and Dowling, 1992; United States government (U.S. Department of Echelle and Echelle, 1993). the Interior, 1986). In this paper, we use mito- chondrial DNA (mtDNA) variation to describe MATERIALS AND METHODS the genetic structure of populations tradition- ally classified as C. macularius and to provide a In 1997-1998, collections of the desert pup- basis for recommendations regarding conser- fish complex were made at 11 sites (n = 19-25) vation genetics of the species. The results, to- representing all major populations (Fig. 1; Ap- gether with geological history and color pat- pendix). We also included 33 specimens from a terns in nuptial males, indicate that populations captive population at Dexter National Fish grouped as C. macularius represent two evolu- Hatchery and Technology Center (DNFH) in tionarily divergent entities that should be rec- New Mexico. Specimens were initially frozen in ognized as separate species. We hereafter refer liquid nitrogen or on dry ice and stored in the to the two species as the "desert pupfish com- lab at -75 C until processed for analysis. plex." DNA was extracted from muscle tissue follow- The historic range of the desert pupfish com- ing the method of Longmire et al. (1997), and plex once extended from Gila River tributaries the polymerase chain reaction (PCR) and sin- in southeastern Arizona and northern Sonora, gle-stranded conformational polymorphism westward to the Salton Sea area of southern Cal- (SSCP) analysis (Orita et al., 1989; Fan et al., ifornia and southward into the Colorado River Delta region in Sonora and Baja California (Miller, 1943). Across this region, Miller and Fuiman (1987) recognized one wide-ranging California 114• C. m. macularius, and a local endem- Salton Arizona subspecies, SSea ic, C. m. eremus, restricted to Quitobaquito 2 3 o ef Springs, Organ Pipe Cactus National Monu- GO ment, southern Arizona. The wide-ranging sub- species has disappeared from the Gila and lower Colorado River areas of Arizona/California Baja 1973; and the remain- 467 6 (Minckley, Moyle, 1976), California 8 *10320 natural are much smaller and ing populations S9 onora 11 more fragmented than in earlier times (Hen- 0 50 100 drickson and Varela, 1989; Dunham and Minck- Km -A ley, 1998). This decline is a result of interactions with introduced and habitat losses re- species 1. Localitiessampled for mtDNAvariation in from reservoir surface-wa- Fig. sulting construction, the desert pupfish complex. Sample sites represent ter diversion projects, groundwater depletion, the three majorareas occupied by extant populations: and other factors (Miller and Fuiman, 1987; the Salton Sea area (sites 1-3), the Colorado River Shoenherr, 1988; Hendrickson and Varela, Delta (sites 4-9), and the Rio Sonoyta/Quitobaquito 1989). Springs area. (sites 10 and 11). Now-extirpatedpop- Previous studies of variation in the ulations are known to have occurred in waters asso- genetic River in Arizona and desert have been restricted to ciated with the lower Colorado pupfish complex from the Gila River Basin at scattered localities from populations in the United States (Turner, near the confluence with the Colorado River to the 1984), or they
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