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Natural Hybridization Between the Teiid Lizards Cnemidophorus Sonorae (Parthenogenetic) and Cnemidophorus Tigris (Bisexual)

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Natural Hybridization Between the Teiid Lizards Cnemidophorus Sonorae (Parthenogenetic) and Cnemidophorus Tigris (Bisexual) NATURAL HYBRIDIZATION BETWEEN THE TEIID LIZARDS CNEMIDOPHORUS SONORAE (PARTHENOGENETIC) AND CNEMIDOPHORUS TIGRIS (BISEXUAL) CHARLES H. LOWE, JOHN W. WRIGHT, CHARLES J. COLE, AND ROBERT L. BEZY Abstract Lowe, Charles H. (Dept. Biological Sciences, Univ. Arizona, Tucson, Arizona 85721), et al., 1970. Natural hybridization between the teiid lizards Cnemidophorus sonorae (parthenogenetic) and Cnemidophorus tigris (bisexual). Syst. Zool, 19:114-127.—Hybrid Downloaded from index analysis of two natural hybrids between the parthenogenetic Cnemidophorus sonorae and the bisexual C. tigris demonstrates that the hybrids more strongly resemble the maternal parent. Karyotypic analysis reveals that the hybrids are tetraploids having received three genomes from the maternal (triploid) species and one genome from the paternal (diploid) species. Examination of testicular material shows the formation of chromosomal bivalents and polyvalents, including quadrivalents. Karyotypic variation http://sysbio.oxfordjournals.org/ involving centric fission occurs in the maternal parent C. sonorae. The origin of various levels of polyploidy in the genus Cnemidophorus appears to be rather different from that occurring most frequently in plants. [Hybridization. Polyploidy. Cnemidophorus. Karyo types.] Formation of species in the whiptail miles SSE of Tucson. It is desert-grassland lizard genus Cnemidophorus presumably (mesquite type, Fig. 1) at an elevation of has occurred generally by means of classi- 3750 feet. Around the butte Cnemidoph- cal mechanisms of allopatric speciation. In orus tigris is by far the most abundant addition, speciation has occurred through whiptail; C. sonorae and C. uniparens occur at Penn State University (Paterno Lib) on September 12, 2016 interspecific hybridization (Lowe and in much fewer numbers and are largely Wright, 1966a, b), which has provided the restricted to riparian situations and open vehicle for an unusually large amount of (non-mesquite) grassland. evolution in the genus. Parthenogenesis The first hybrid was obtained while and utilization of "weed" habitats are im- shooting a sample of lizards around the portant cofactors in the survival of hybrid butte. Its general appearance was that of forms (Wright and Lowe, 1968). Further- an aberrant C. sonorae; this combined with more, triploid species have evolved as a its possession of hemipenes suggested a consequence of hybridization between dip- hybrid. On the following day a second loid parthenogenetic forms and diploid hybrid was noosed which provided the bisexual forms (Lowe and Wright, 1966a, necessary living material for karyotypic b). We report here on natural hybrid- analysis. This cytogenetic analysis verified ization between a triploid parthenogenetic the hybrid origin of the specimen (See species (Cnemidophorus sonorae) and a KARYOTYPES below). diploid bisexual species (Cnemidophorus Today this locality is a hybrid habitat, tigris), resulting in the production of in the sense of Anderson (1948, 1949), tetraploid individuals in a "weed" habitat where the present desert-grassland has only in southern Arizona. recently appeared—mostly during the pres- ent century through a series of environ- HYBRID HABITAT mental changes before and after the turn Two hybrids (Cnemidophorus sonorae of the century. In this hybridization of the X C. tigris) were collected July 2-3, 1966, habitat, the ecologic transformation has at the SE base of Huerfano Butte on the clearly favored desert species (Fig. 2). Santa Rita Experimental Range, Pima The importance of such hybrid habitats in County, Arizona. The locality is 27 airline hybridization and evolution in the genus 114 NATURAL HYBRIDIZATION IN CNEMIDOPHORUS 115 Downloaded from http://sysbio.oxfordjournals.org/ at Penn State University (Paterno Lib) on September 12, 2016 -*% •&kt&fa> <f FIG. 1.—Desert-grassland hybrid habitat at south base of Huerfano Butte, Pima County, Arizona. Trees are primarily mesquites (Prosopis juliflom). Locality of hybridization of Cnemidophorus sonorae (parthenogenetic) and C. tigris (bisexual). Photo by Oscar H. Soule, July 3, 1966. Cnemidophorus has been recently discussed between the paravertebral light stripes; elsewhere (Wright and Lowe, 1968). SPV/SAB X 100, ratio of above two char- acters; FP, femoral pores; TLS, toe lamellar HYBRID INDEX scales; PBS/DS, postantebrachial scale The results of our investigation of the diameter/dorsal scale diameter; MS/DS, external morphology of the parental series mesoptychial scale width/dorsal scale diam- of Cnemidophorus tigris (N = 51) and C. eter; COS, circumorbital semicircle scales; sonorae (N = 19) from Huerfano Butte, and ILS, interlabial scales. Except for the ratios the two hybrids obtained with them, are PBS/DS and MS/DS, used here for the summarized in Tables 1 and 2. Table 1 first time, standardizations for the measure- provides the hybrid indexes for each of the ment of the characteristics above are dis- two hybrids; these indexes are based on cussed in Wright and Lowe (1967). the data reductions that are given in Table PBS/DS.—As an estimate of the degree 2 for the two parental species. The female of enlargement of the postantebrachials, species (C. sonorae) is set at 100, and the the ratio (PBS/DS) of the diameter of bisexual species (C. tigris) at 0, on the these scales to that of the dorsal scales was percent scale in the hybrid index of Hubbs, calculated. The maximum diameter of the Hubbs, and Johnson (1943); see Wright largest postantebrachial scale was mea- and Lowe (1967). sured to the nearest 0.06 mm, using an Abbreviations are as follows: SAB, scales ocular micrometer. The size of the mid- around body at ventral row 15; SPV, scales dorsal scales (DS) was taken as the mode 116 SYSTEMATIC ZOOLOGY Downloaded from http://sysbio.oxfordjournals.org/ FIG. 2.—UPPER. Circa 1902. Looking WSW toward Huerfano Butte, Pima County, Arizona. Mesquite {Prosopis juliflora) is identifiable on the bajada, as is cane cholla (Opuntia spinosior). The conspicuous shrubs on the rock slope are primarily desert hackberry (Celtis pallida) and desert-thorn at Penn State University (Paterno Lib) on September 12, 2016 (Lycium andersoni). LOWER. March 16, 1969. Same view as above approximately 67 years later, showing marked vegetation change to well-defined desert-grassland at this hybrid locality. The trees, shrubs, and cacti (which, with the grasses, comprise 90-100% of the perennial cover) in the fore- ground are: mesquite (Prosopis juliflora), desert hackberry (Celtis pallida), burro-weed (Aplopappus tenuisectus), barrel cactus (Echinocactus wislizenni), prickly-pear (Opuntia engelmanni), cane cholla (Opuntia spinosior), and jumping cholla (Opuntia fulgida). Detail of the site of collection of the hybrids on the left base of Huerfano Butte is shown in Fig. 1. Photo by Charles H, Lowe. NATURAL HYBRIDIZATION IN CNEMIDOPHORUS 117 of the maximum diameters of five body TABLE 1. HYBRID INDEXES FOR TWO MALE HY- scales along the paravertebral stripe above BRIDS (C. sonorae X C. tigris) AT HUERFANO BUTTE the 15th ventral. IN SOUTHERN ARIZONA. MS/DS.— The maximum width of the Hybrid Hybrid Charac- C. UAZ UAZ largest mesoptychial scale (MS) bordering teristic tigris 24953 24954 sonoraec. the gular fold was measured to the nearest Sex $, 5 $ $ 29 0.06 mm, with an ocular micrometer. The N 20-51 1 1 17-19 ratio (MS/DS) of the size of the mesopty- SAB1 chials to that of the dorsal scales was then SPV 0 142 103 100 Downloaded from calculated; for measurement of DS, see SPV/SAB x 100 0 129 86 100 FP1 above. TLS 0 165 165 100 That both hybrids possess a phenotype PBS/DS 0 43 58 100 significantly more similar to that of C. MS/DS 0 90 90 100 sonorae than to that of C. tigris is clearly COS 0 -25 + 17 100 http://sysbio.oxfordjournals.org/ evident in both their overall appearance ILS 0 57 36 100 (Fig. 3) and in their high hybrid indexes Color Pattern (Table 1). Such high hybrid indexes may Dorsal 0 75 75 100 Ventral 0 100 100 100 be expected in this case, inasmuch as C. sonorae is a triploid parthenospecies and Mean 0% 86% 81% 100% C. tigris is diploid. The calculated index 1Foi each of two characteristics (SAB, FP), the differ- values are 81% and 86%, based on nine ence between the means for the parental frequency distri- butions is not significant (P>.20; P>.10, respectively); morphological characteristics for each of therefore, a meaningful hybrid index cannot be established for these characteristics, and such values are not given. two hybrids (Tables 1 and 2). This simi- at Penn State University (Paterno Lib) on September 12, 2016 larity of the tetraploid hybrid to its triploid female parent is largely due to the maternal used for Cnemidophorus by Lowe and contribution of three genomes in contrast Wright (1966b); Set I = large metacentrics to the paternal contribution of one genome. and submetacentrics, Set II = medium sub- Further, it is undoubtedly this strong metacentrics, subtelocentrics, and telo- resemblance to one of the parents that has centrics, and Set III = small chromosomes led to misinterpretation of hybrids as being (microchromosomes). males of all-female species of Cnemi- dophorus, as discussed below. Cnemidophorus sonorae.—The Sonora spotted whiptail is a triploid unisexual ("all-female") species for which we have KARYOTYPES found thus far three karyotypes in the im- Preparations of chromosomes were made mediate vicinity of Huerfano Butte. Indeed, following Patton's (1967) hypo-tonic cit- we have found minor intraspecific karyo- rate, air-dried technique, slightly modified typic variation to be the general rule (Lowe, Wright, and Cole, 1966). Chromo- specifically among the triploid all-female somes were examined in detail in a total species of Cnemidophorus, which appar- of more than 145 cells (bone marrow and ently tolerate chromosomal aberrations testicular preparations) from 14 individuals considerably more so than their diploid of C. tigris and 5 of C. sonorae, plus 24 bisexual congeners. additional cells (bone marrow and testic- The karyotypes of C. sonorae (Figs. 4- ular preparations) from a hybrid male 5) are composed basically of three haploid (see list of specimens examined, below).
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