Apparent Natural Hybridization Between the Rattlesnakes Crotalus atrox and C.

horridus
Author(s): Jesse M. Meik, Brian E. Fontenot, Carl J. Franklin, and Clint King Source: The Southwestern Naturalist, 53(2):196-200. 2008. Published By: Southwestern Association of Naturalists DOI: http://dx.doi.org/10.1894/0038-4909(2008)53[196:ANHBTR]2.0.CO;2 URL: http://www.bioone.org/doi/ full/10.1894/0038-4909%282008%2953%5B196%3AANHBTR%5D2.0.CO %3B2

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THE SOUTHWESTERN NATURALIST 53(2):196200

JUNE 2008

APPARENT NATURAL HYBRIDIZATION BETWEEN THE RATTLESNAKES CROTALUS ATROX AND C. HORRIDUS
JESSE M. MEIK,* BRIAN E. FONTENOT, CARL J. FRANKLIN,
AND

CLINT KING

Department of Biology, The University of Texas at Arlington, Arlington, TX 76019 ( JMM, BEF) Amphibian and Reptile Diversity Research Center, The University of Texas at Arlington, Arlington, TX 76019 (CJF) 235 North Cardinal Road, Azle, TX 76020 (CK) *Correspondent: jmeik@uta.edu
ABSTRACTWe used scalation, color pattern, and scanning electron microscopy of scale microdermatoglyphics to evaluate the hypothesis that an unusual rattlesnake specimen, from Wise Co., Texas, represents a natural hybrid between Crotalus atrox and C. horridus. The specimen demonstrates particular features of scalation and color pattern that are characteristic of either, but not both, parental species. With respect to microstructure of scales, the specimen exhibits a phenotype intermediate between the putative parental species. Based on this evidence, we tentatively consider the specimen to represent the first reported natural hybrid between C. atrox and C. horridus. RESUMENUtilizamos escamacio n, patro n de coloracio n, y microscopia electro nica de microdermatoglifos de escamas para evaluar la hipo tesis de que un espe cimen inusual, colectado en el condado de Wise, Texas, representa un h brido natural entre Crotalus atrox y C. horridus. Este espe cimen muestra algunas caracter sticas de escamacio n y patro n de coloracio n que son distintivas de una u otra, pero no de ambas, especies parentales. Con respecto a la microestructura de escamas, el espe cimen exhibe un fenotipo intermedio entre las supuestas especies parentales. Basa ndonos en esta evidencia, tentativamente consideramos el espe cimen como el primer registro de un h brido natural entre C. atrox y C. horridus.

Together, the western diamondback rattlesnake (Crotalus atrox) and the timber rattlesnake (C. horridus) are widely distributed in North America; C. atrox is primarily in the southwestern United States and throughout northern Mexico, while C. horridus occurs in the eastern and central United States (Campbell and Lamar, 2004). Although the respective distributions and habitats occupied are largely mutually exclusive, the species do occur in limited sympatry in Texas, Oklahoma, and Arkansas. Natural hybridization between C. atrox and C. horridus has not been reported previously; indeed, natural hybridization between species of rattlesnakes has been documented only rarely (e.g., #10 verified instances; see review in Campbell and Lamar, 2004). The documentation of natural instances of hybridization is important as such events may have far-reaching implications regarding mechanisms of speciation and evolution of reproductive barriers (Coyne and Orr, 2004). Herein, we report an aberrant specimen of Crotalus that was collected 16 September 2003

from Wise Co., Texas (UTA R-52942; AOR on FM 1655 ca. 6.7 mile N Hwy 380; Fig. 1). This specimen is distinctive in that it appears to possess elements of color pattern intermediate between C. atrox and C. horridus, both of which have been collected from Wise County. Previously, Campbell et al. (1989) used scanning electron microscopy and other morphological comparisons to identify a natural hybrid between C. willardi and C. lepidus. The objective of our study was to follow the methods of Campbell et al. (1989) in evaluating the hypothesis that the unusual specimen obtained from Wise County represents a hybrid. We also provide a brief description of the putative hybrid, as it may prove useful to future studies. MATERIALS AND METHODSUse of morphological evidence to identify hybrids is constrained in that only characters that differ between parental species generally are informative. For a specific character, hybrids may demonstrate traits of either parental species or, alternatively, an intermediate condition. Taken together, it is the expression of various character states from

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FIG. 1Photograph of putative hybrid (UTA R-52942) between Crotalus atrox and C. horridus from Wise Co., Texas. either parental species, intermediate character states, or both, that contributes to the intermediate phenotype of the hybrid individual. Crotalus atrox and C. horridus overlap broadly in the majority of standard scale counts, making identification of hybrids based on scalation difficult. Intraspecific variation can add further complexity in identifying characters as intermediate; thus, our approach was to focus on identifying traits in the hybrid that were typical of either, but not both, parental species. Comparisons of external scalation and color pattern were made between the apparent hybrid and the supposed parental species. Apart from C. atrox and C. horridus, the only rattlesnakes known to occur in Wise County are Sistrurus catenatus and S. miliarius. The apparent hybrid is sufficiently distinct from either of these relatively distantly related species to preclude the possibility that they may represent parental species. We examined specimens of C. atrox (UTA R-15653, 15654) and C. horridus (UTA R-22357; UTA R-54136) from Wise County and adjacent Cooke County, and referred to Campbell and Lamar (2004) for distribution-wide summaries of data. Dorsal scales were collected from preserved specimens of C. atrox, C. horridus, and the putative hybrid following the procedure of Gutberlet (1998). All dorsal scales were collected from the midbody region close to the vertebral column. We removed scales by gently pressing against a single dorsal scale until the thin outer layer was separated. Removed layers of scales were then placed in 95% ethanol and sonicated for 10 min to remove external debris. We then dried scales overnight in an oven set to 70uC. Dehydrated scales were placed on microscope stubs with double-sided tape and sputter coated with a thin layer of goldpalladium in a Hummer VI sputter coater. A JEOL 35 C scanning electron microscope, housed in the University of Texas at Arlington Center for Electron Microscopy, was used to examine surfaces of scales. Surfaces of scales were examined at magnifications of 150, 1,200, 1,500, 2,000, and 3,0003.

RESULTS AND DISCUSSIONComparison with parental speciesThe putative hybrid exhibits individual scalation and color-pattern traits that are typical of either C. atrox or C. horridus from northern Texas (Table 1). Overall, the specimen resembles C. horridus in salient aspects of head pattern and scalation, and more closely resembles C. atrox in dorsal body pattern. Color pattern of tail and condition of lateral facial markings are two characters that reliably distinguish C.

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TABLE 1Comparison of scalation and color pattern traits between Crotalus atrox, C. horridus, and a putative hybrid specimen from Wise Co., Texas. Character Loreals Interoculabials Tail coloration Venter pattern Paired parietal spots Vertebral stripe Postocular stripe White postocular-stripe borders Dorsal body pattern C. horridus Paired 13 Uniform black Mottled Present Present Extends beyond rictus Absent Narrow crossbands Hybrid (UTA R-52942) Paired 3 Black and white rings Mottled Present Absent Extends beyond rictus Absent Broad blotches C. atrox Single 12 Black and white rings Immaculate Absent Absent Does not reach rictus Present Broad blotches

atrox from C. horridus; the putative hybrid has black and white bands on the tail (characteristic of C. atrox), but the distinctive white scales that abut the anterior and posterior borders of the postocular stripe in C. atrox are absent (characteristic of C. horridus). The putative hybrid has a dorsal body pattern that consists of closely spaced rhomboid or diamond-shaped blotches, similar to C. atrox from the region. Although C. horridus from the northeastern United States may also have a similar blotched pattern, specimens from northern Texas generally have narrow, irregular crossbands separated by broad interspaces. With respect to scanning electron microscopy of scales, all specimens exhibited coarse microstructure consistent with other species of Crotalus (Stille, 1987). This coarse microstructure consists of rounded hillocks demarcated by the boundaries of oberhautchen cells. Differences were mostly in rugosity of these hillocks, with C. atrox characterized by low, moderately foveate hillocks (Fig. 2a), C. horridus characterized by rugose, distinctly foveate hillocks (Fig. 2c), and the putative hybrid characterized by slightly rugose, weakly foveate hillocks (Fig. 2b). Fine microstructure of all specimens was consistent with other species of Crotalus (Stille, 1987). Crotalus atrox was characterized by a uniform vermiculate pattern nested inside hillocks of the dorsal scales (Fig. 2a). Crotalus horridus was characterized by a spinulate pattern nested inside hillocks of the dorsal scales, with small pits non-uniformly interspersed across the surface of scales (Fig. 2c). The putative hybrid exhibited a pitand-groove pattern, with long, irregularly shaped vermiculate grooves and porous regions near boundaries of the oberhautchen cells (Fig. 2b).

Levels of intraspecific variation in microdermatoglyphics of dorsal scales observed among specimens in this study were minimal. Both coarse and fine microstructure in the putative hybrid suggested an intermediate condition; coarse microstructure is raised higher than that of C. atrox and lower than that of C. horridus, whereas fine microstructure shows irregular grooves (similar to C. atrox) and intermittent pits (similar to C. horridus). Collectively, the data gathered from scalation, color pattern, and microdermatoglyphics of scales are consistent with the hypothesis that UTA R-52942 represents a natural-hybrid specimen. Our conclusion is necessarily tentative, as hybrids cannot unequivocally be identified without direct knowledge of parentage. Inferences of parentage could be made using molecular data; however, we were unable to obtain tissue samples of the hybrid prior to preservation. Description of hybridThe hybrid is a subadult female with a snoutvent length of 667 mm and a tail length of 38 mm. In preservative, ground color is gray (in life ground color was pale brown with a greenish cast); the 32 middorsal blotches are rhomboid or diamond-shaped anteriorly, and merge with lateral series to form crossbands near the tail. Blotches are brown with pale centers and are bordered by dark scales, white edging is present on most blotches, and no interspaces are present between the middorsal blotches, except for the posterior one-third of the body where one or two rows of dorsal scales may interrupt contact of the series. Two series of smaller blotches are present on the sides; the dorsolateral series is faint and the ventrolateral series is distinct and aligned with the primary middorsal blotches. Venter is mottled. Tail has

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FIG. 2a) Dorsal scale of Crotalus atrox (UTA R15653); b) dorsal scale of putative hybrid (UTA R52942); c) dorsal scale of C. horridus (UTA R-22357). All images are at 1,2003 magnification.

four black rings with ash-white interspaces, the interspaces are about two-thirds the length of the black rings. The rattle is broken, with only three remaining segments. Two elongated occipital blotches are on the head near the juncture with the neck. Two small spots are in the parietal region; the remainder of the crown is faintly dusted with brown pigment. A broad postocular

stripe extends from the lower edge of the eye to well beyond the rictus of the mouth, with a gap in the dark pigment immediately above the ultimate and penultimate supralabials. The rostral is higher than wide. There are two internasals in contact with the rostral, 19 scales in the internasal-prefrontal region (including canthals and internasals), a minimum of 5 intersupraoculars, and 33 interrictals. Prenasal is in contact with the supralabial series. Postnasal-preocular contact is precluded by presence of paired loreals. There are 6/7 prefoveals, 2/2 preoculars, 3/3 interoculabials, 15/15 supralabials, 17/18 infralabials, 31-25-21 dorsal scale rows, 180 ventrals, 21 subcaudals, and 12 rattlefringe scales. RemarksSpecimens of rattlesnakes catalogued as hybrids are common in herpetological collections across the United States implying that natural hybridization among various species of rattlesnakes may be a frequent event. However, in most instances, status of these specimens as hybrids has yet to be adequately determined and many are likely not of hybrid origin. Instances of natural hybridization in rattlesnakes have been documented for the following crosses: C. viridis 3 C. scutulatus (Murphy and Crabtree, 1988), C. adamanteus 3 C. horridus, C. ruber 3 C. oreganus (Klauber, 1972), C. lepidus 3 C. willardi (Campbell et al., 1989), C. scutulatus 3 C. molossus, and C. atrox 3 C. scutulatus (Campbell and Lamar, 2004). A possible intergeneric hybridization event between S. catenatus and C. horridus also has been reported (Bailey, 1942). The hybrid specimen described herein was collected near Lyndon B. Johnson National Grasslands in a biogeographic province known as the Western Cross Timbers, a region characterized by post-oak woodland and mixed-grass prairie. Over the past century, natural vegetation of the Western Cross Timbers has become increasingly fragmented as more land is converted to agricultural use (Schmidly, 2004). This shift in vegetation and land use undoubtedly has influenced distributions and abundances of native herpetofauna. The most common effects of habitat modification include reduction in genetic diversity and alterations in genetic structure of populations of species inhabiting affected areas (Arnold, 1997). A common secondary effect of habitat modification is an increase in opportunities for natural hybridization, particularly in cases where one species is

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less common than the other (Arnold, 1997). While data from other regions suggest that C. atrox may have a mixed, or even favorable, response to habitats modified by human activity (Mendelson and Jennings, 1992), it is likely that populations of C. horridus in northern Texas are in decline. The synergistic effects of habitat modification and presence of a potentially more numerous, reproductively compatible congener in direct contact with C. horridus could have serious implications for conservation. Vegetative changes brought about by human use of land may result in an unstable dynamic where two species that historically do not occur in the same habitat (such as C. atrox and C. horridus) are increasingly found in syntopy, which could lead to increased natural-hybridization events, outbreeding depression, and genetic assimilation of the rarer species (Ellstrand, 1992; Arnold, 1997). While it is likely that the hybrid individual described herein represents an isolated instance of natural hybridization between C. atrox and C. horridus, it is possible that hybridization events between these species could become more common as habitat modification increases.
We thank K. Beaman for providing important information regarding hybridization in rattlesnakes and J. Campbell and W. Schargel for comments on an early version of the manuscript. We also thank H. J. Arnott and M. Gracey for valuable assistance with the scanning electron microscope.

LITERATURE CITED
ARNOLD, M. L. 1997. Natural hybridization and evolution. Oxford University Press, New York.

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