Natural Hybridization Between the Teiid Lizards Cnemidophorus tesselatus (Parthenogenetic) and C. tigris marmoratus (Bisexual): Assessment of Evolutionary Alternatives

Abstract Annual hybridization is taking place between representatives of the parthenogenetic lizard Cnemidophorus tesselatus (2n = 46, 47) and males of the bisexual species C. tigris marmoratus (2n = 46) in desert grassland habitats at Arroyo del Macho, Chaves County, New Mexico. This raises the question of whether a new triploid parthenogenetic species may be originating as a consequence of this activity. Hybrids were collected in each of four years (1996–1999), and 20 of 21 hybrids collected (12 males and 8 females) were available for study. Although a triploid parthenogenetic species (Cnemidophorus exsanguis 3n = 69) and a diploid bisexual species (C. inornatus 2n = 46) were also found at the hybridization site, the genealogy of the hybrids was determined unequivocally with karyotypic and electrophoretic evidence (34 loci tested). The specimens examined electrophoretically included an adult female and one of her laboratory-reared daughters, which demonstrated for the first time clonal inheritance in C. tesselatus pattern class E. The population of C. tesselatus at Arroyo del Macho is characterized by two karyotypic cytotypes. The ancestral one (2n = 46) occurs at about half the frequency of the derived cytotype (2n = 47), which apparently was produced by centric fission of the ancestral X-chromosome from C. tigris In contrast, the occurrence of the two cytotypes was reversed and strongly asymmetrical in the hybrids; only one of nine hybrids possessed the fissioned X-chromosome. This individual was significantly different in 12 meristic characters from the sample of hybrids with intact X-chromosomes. Predictably, principal components scores for this individual fell outside the 95% confidence ellipse of scores of the other eight hybrids that were karyotyped. The skewed ratio and multiple phenotypic differences suggest that hybrids inheriting a fissioned X-chromosome might be at a selective disadvantage compared to hybrids with intact X-chromosomes. All 20 hybrids closely resemble C. tesselatus in most color pattern features. However, these hybrids, like C. tigris marmoratus lack lateral stripes. Because the population of C. tesselatus at Arroyo del Macho has lateral stripes (or their remnants), hybrids can be readily distinguished from C. tesselatus by this color pattern feature. Compared to the two parental species, hybrids had a significantly lower mean number of scales around midbody, but hybrids resembled either C. tesselatus or C. tigris marmoratus in other univariate meristic characters. This mosaic pattern of resemblance was simplified to a three-dimensional depiction of variation using principal components analysis. Each of two principal components expressed the resemblance of hybrids to one of the two parental species. A third component reflected the difference between hybrids and both parental species. A canonical variate analysis of meristic characters demonstrated the multivariate distinctiveness of each group—hybrids, C. tesselatus and C. tigris marmoratus However, based on Mahalanobis D2 distances, the closest morphological resemblance among hybrids and parental species was between hybrids and the maternal species, C. tesselatus Nine additional museum specimens, suspected of being C. tesselatus × C. tigris marmoratus hybrids, were identified, as such, by a canonical variate analysis using our samples of C. tesselatus, C. tigris marmoratus and hybrids from Arroyo del Macho as a priori groups. These nine individuals document hybridizations between C. tesselatus and C. tigris marmoratus at two additional localities in Chaves County, New Mexico, two localities in Sierra County, New Mexico, and a cluster of sites near Presidio, Presidio County, Texas. Previously, several of these hybrids had been misidentified as male C. tesselatus The reproductive systems of female and male hybrids were compared histologically to those of C. tesselatus and C. tigris marmoratus respectively. Sexually mature and reproductive adults of C. tesselatus usually have oocytes in the ovary, complete and well-organized ovarian follicle walls, inconspicuous connective tissue and fewer vacuoles in the well-vascularized ovary, the distal oviduct with a thin mucosa, well-developed alveolar glands restricted to the middle oviduct, a proximal oviduct with a thick mucosa and well-developed folds, and small mesonephric tubules. Female hybrids have a poorly defined follicular epithelium with little vascularization in small ovaries, empty or fluid-filled follicles without oocytes, few or no cilia in the middle oviduct, and numerous abnormally large mesonephric tubules. There is no evidence that Cnemidophorus tesselatus × C. tigris marmoratus females can produce viable and fertile eggs. Although hybrid males are capable of producing sperm that appear normal and were present in the epididymides, the allotriploid chromosome complement reduces the chance that sperm would carry genetically balanced sets of information. Although the annual production of hybrids could affect the long-term success of this local population of C. tesselatus two lines of evidence indicate that hybridization is unlikely to result in its extirpation. First, the population of C. tigris marmoratus at Arroyo del Macho is tightly associated with a microhabitat dominated by creosote bush. Because creosote bush is distributed there in small, widely scattered patches, the density of C. tigris marmoratus is relatively low, and many individuals of C. tesselatus escape insemination. This was evident from an absence of sperm in the reproductive tracts of 11 individuals of C. tesselatus collected during the peak reproductive season (May and June) of three different years. Second, reproductively mature individuals of C. tesselatus are significantly larger than comparable females of C. tigris marmoratus This translates into larger clutches, with the mean clutch size of C. tesselatus being twice as large as that of C. tigris marmoratus The disparity in mean clutch size in conjunction with habitat constraints on C. tigris marmoratus probably explains why C. tesselatus outnumbers both C. tigris marmoratus and hybrids by a ratio of approximately 2:1 at the hybridization site. Although hybridization between C. tesselatus and C. tigris marmoratus appears to be an annual event at Arroyo del Macho, there is no evidence that a new triploid parthenogenetic species is resulting from this hybridization activity—all female hybrids examined were sterile. Nevertheless, the hybridization taking place at Arroyo del Macho is a remarkable natural experiment in progress, with either evolutionary alternative—speciation vs. destabilizing hybridization—adding to an understanding of the dynamics between parthenogenetic and bisexual species in sympatric associations.