Neaves' Whiptail Lizard: the First Known Tetraploid Parthenogenetic
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US ISSN 0006-9698 CAMBRIDGE,MASS.5DECEMBER 2014 NUMBER 539 NEAVES’ WHIPTAIL LIZARD: THE FIRST KNOWN TETRAPLOID PARTHENOGENETIC TETRAPOD (REPTILIA: SQUAMATA: TEIIDAE) CHARLES J. COLE,1 HARRY L. TAYLOR,2 DIANA P. BAUMANN,3 AND PETER BAUMANN4 ABSTRACT. The first known tetraploid amniote that reproduces through parthenogenetic cloning by individual females is named and described. The species originated through hybridization between Aspidoscelis exsanguis (triploid parthenogen) 3 Aspidoscelis inornata (diploid bisexual or gonochoristic species) in the laboratory. We compared multivariate morphological variation between two lineages that arose from separate F1 hybrid zygotes in one clutch and among several generations in those lineages. The tetraploid species is also compared with its ancestral taxa, with two hybrids of A. exsanguis 3 A. inornata that were found in nature at two localities that are 100 km apart in southern New Mexico, and with three laboratory hybrid males. This will facilitate identification of field-caught tetraploids in the future. KEY WORDS: Aspidoscelis neavesi; new species; tetraploid; parthenogenesis; clonal lineages INTRODUCTION in the absence of spermatozoa) occurs as the normal mode of reproduction in only a few Among amniotes, true parthenogenesis species, all of which are reptiles (several (initiation and completion of embryogenesis lizards and apparently one snake; reviewed in Dawley and Bogart, 1989; Lutes et al., 1 Division of Vertebrates (Herpetology), American 2011; Neaves and Baumann, 2011). Many of Museum of Natural History, 200 Central Park West, these are whiptail lizards (Aspidoscelis), of New York, New York 10024, U.S.A.; e-mail: cole@ which the unisexual (all-female) lineages amnh.org. receive formal recognition as species because 2 Department of Biology, Regis University, Denver, Colorado 80221, U.S.A.; e-mail: [email protected] they are of unique ancestry (reviewed by 3 Stowers Institute for Medical Research, 1000 East 50th Reeder et al., 2002) and individuals repro- Street, Kansas City, Missouri 64110, U.S.A.; e-mail: duce by parthenogenetic cloning (Lutes et [email protected] al., 2010, 2011). Additionally, rare instances 4 Howard Hughes Medical Institute and Stowers Insti- tute for Medical Research, Kansas University Medical of hybridization and fertilization of a par- Center, Kansas City, Missouri 64110, U.S.A.; e-mail: thenogenetic female’s cloned eggs have re- [email protected] sulted in triploid clonal species of unique E The President and Fellows of Harvard College 2014. 2 BREVIORA No. 539 ancestry (e.g., Aspidoscelis exsanguis; re- eral were diagnosed, described, and named viewed by Reeder et al., 2002). Although a well before scientists knew that unisexual, few tetraploid hybrid individuals were re- clonal lizards exist (e.g., Ameiva tesselata [Say ported in the past (Lowe et al., 1970a; in James, 1823:50–51], known today as Neaves, 1971), no tetraploid clonal lineages Aspidoscelis tesselata). Each clone with a were known until Lutes et al. (2011) reported distinctive ploidy and distinctive combination the laboratory origin of the species for which of ancestral genomes has been named, reflect- we provide a name, morphological descrip- ing its unique historical origin (reviewed in tion, and both intraspecific and interspecific Reeder et al., 2002). Additionally, some comparisons here. clones with distinctive scalation and/or color- Aspidoscelis is a genus of North American ation derived as a consequence of postforma- whiptail lizards that includes several unisex- tional mutations have been named even ual (all-female), parthenogenetic species as though they share a common hybrid origin well as gonochoristic species (reviewed by with other clones (e.g., Aspidoscelis maslini Reeder et al., 2002). All of the unisexual Fritts, 1969, versus other clones of the species ultimately had a hybrid origin, the Aspidoscelis cozumela complex; Taylor et al., females clone themselves, and the primary 2005). Coauthors of the present paper differ lineages bear formal binomials, although in philosophy and practice on this point, but derived clonal lineages with postformational in general, we do not favor naming post- mutations usually do not. Although the formational clones but prefer to treat them as International Code of Zoological Nomencla- a complex of derivative forms under one ture (ICZN, 1999) prohibits naming hybrids specific epithet (e.g., the A. tesselata com- (Article 1.3.3), this restriction applies to plex), which clearly reflects their relation- individual animals that are hybrids between ships. This is similar to recognizing that two species, not self-perpetuating clonal extensive genetic variation occurs within entities that are unique evolutionary lineages. named species of gonochoristic taxa. In the case of unisexual species of Aspidosce- In this paper we name, diagnose, and lis, historically, the F1 hybrid females estab- describe a unique unisexual species of hybrid lished continuing lineages by cloning them- origin. It is the first tetraploid vertebrate selves parthenogenetically, and the offspring known to clone itself parthenogenetically continued to reproduce as did their mother. and it is reproductively isolated from all This quantum leap in evolution (the switch other species (Lutes et al., 2011). The name, from spermatozoan-dependent to spermato- given below, will provide for efficient, effec- zoan-independent reproduction) occurred in tive, and unambiguous communication, par- each case in just one generation (reviewed by ticularly for tracking data among various Reeder et al., 2002). In such lineages, individ- publications, as this model organism is being uals of the F2 and subsequent generations are used for considerable research on basic not hybrids but clones of their single parent. biological processes (e.g., molecular aspects In recognition of this, ICZN (1999) adopted of meiosis; Lutes et al., 2010, 2011) and DNA Article 17.3, validating the naming of parthe- sequencing, which involves listing in on-line nogenetic entities of hybrid origin. data information services such as GenBank, Some clonal lineages of hybrid origin are RefSeq, and UniProt. morphologically cryptic species, but many Although the presently known reproduc- have distinctive morphologies in size, color ing lineages of this tetraploid species origi- pattern, and/or scalation. Consequently, sev- nated in the laboratory by hybridization 2014 NEAVES’ WHIPTAIL LIZARD 3 between the triploid parthenogenetic A. mother of each egg clutch is noted (as is the exsanguis (R) and Aspidoscelis inornata (=; father, if applicable), hatchlings are noted as a diploid bisexual species), this same combi- to clutch, and throughout life, individuals nation of chromosomes was found in a are photographed periodically and tracked tetraploid female (MCZ 101991) from Ala- as to which enclosures they occupy at any mogordo, Otero County, New Mexico, in time. Lineage membership is confirmed using 1967 by William B. Neaves, and the female microsatellite DNA analysis (e.g., Lutes et laid eggs in captivity (Neaves, 1971). At the al., 2011). time, however, the female oviposited in dry Morphological Characters Examined. These sand, and the eggs became desiccated and are listed in Appendix 1, and specimens were discarded, although otherwise they examined are in Appendix 2. Nomenclature looked normal. A second relevant specimen for epidermal scales follows Smith (1946). Sex (UCM 29196) was found near Mesilla, Dona was determined by dissection and examina- Ana County, New Mexico (Taylor et al., tion of primary sexual characters, a history of 1967). This one was a male and was oviposition, or examination of external sec- identified as representing the all-female A. ondary characters. exsanguis. However, we hypothesize that this Museum abbreviations for specimens exam- specimen is also a tetraploid of hybrid origin ined: AMNH, American Museum of Natural between A. exsanguis and A. inornata, because History, New York, New York; MCZ, eggs of whiptail lizards that receive a Y- Museum of Comparative Zoology, Harvard bearing spermatozoan produce males, regard- University, Cambridge, Massachusetts; less of ploidy level (Cole et al., 1969; Lowe et MSB, Museum of Southwestern Biology, al., 1970a; Taylor et al., 2001). We borrowed University of New Mexico, Albuquerque, and examined both of these specimens from New Mexico; SIMR, Stowers Institute for New Mexico and included them in our Medical Research, Kansas City, Missouri; comparisons below. UCM, University of Colorado Museum, In addition to describing the unique Boulder, Colorado. tetraploid species in this paper, we present Multivariate Statistical Analyses. Al- morphological data for individuals of sev- though we had 177 specimens available for this study, we could use only specimens with eral lineages. These were cloned from F1 zygotes of a single pair of parents (A. complete data for the suite of 10 meristic exsanguis 3 A. inornata). We also compare characters analyzed. Therefore, as required samples of two well-represented lineages by the procedures, 65 specimens were ex- with each other (including generation-to- cluded because of one or more damaged or generation comparisons) and compare the missing characters. This left us with the following numbers of specimens for principal tetraploids to samples of their parental components analyses (PCAs) and canonical species and specimens of similar hybrid variate analyses (CVAs): tetraploids (90 of ancestry found in nature. 130); A. exsanguis