Journal of Herpetology, Vol. 39, No. 2, pp. 266–277, 2005 Copyright 2005 Society for the Study of Amphibians and Reptiles
Application of the Evolutionary Species Concept to Parthenogenetic Entities: Comparison of Postformational Divergence in Two Clones of Aspidoscelis tesselata and between Aspidoscelis cozumela and Aspidoscelis maslini (Squamata: Teiidae) HARRY L. TAYLOR,1,2 JAMES M. WALKER,3 JAMES E. CORDES,4
AND
GLENN J. MANNING3
1
Department of Biology (D-8), Regis University, Denver, Colorado 80221, USA; E-mail:
[email protected] 3 Department of Biological Sciences, University of Arkansas, Fayetteville, Arkansas 72701, USA; E-mail (JMW):
[email protected]; (GJM):
[email protected] 4 Division of Sciences, Louisiana State University at Eunice, Eunice, Louisiana 70535, USA; E-mail:
[email protected] ABSTRACT.—Sumner Lake State Park, De Baca County, New Mexico, is the only known locality where three pattern classes of diploid, parthenogenetic Aspidoscelis tesselata (Sumner C, Sumner D, and Sumner E) coexist in syntopy. Reciprocal skin transplants confirmed that the pronounced phenotypic differences between Sumner C and Sumner E represent postformational genetic changes rather than separate hybridization origins. Sumner D is meristically indistinguishable from Sumner C and is considered to be a recent mutational derivative of the latter. In contrast, Sumner E is distinctly different from Sumner C in multivariate meristic characters and several important life-history characteristics. Discordant patterns of phenotypic variation characterize many geographically disjunct groups of A. tesselata classified as pattern class E, thus defying a cohesive diagnosis. Therefore, based on the evolutionary species concept (ESC), we consider Sumner C and Sumner E to be divergent clonal groups in the same species. We contrast this example with a parthenogenetic complex on the Yucata´n Peninsula in which formal recognition of Aspidoscelis maslini and Aspidoscelis cozumela can be accommodated under the ESC.
In a review of theoretical challenges to the long-term success of unisexual vertebrates, Vrijenhoek (1989: 28) noted the absence of documented examples of discrete ecological or morphological groups originating from within ‘‘asexual lineages.’’ However, examples of divergence, sufficiently strong to raise questions of possible formal recognition, occur in parthenogenetic species of the lizard genus Aspidoscelis. For example, diploid Aspidoscelis tesselata shows clonal divergence in color pattern (Zweifel, 1965; Walker et al., 1997), protein phenotypes (Parker and Selander, 1976; Dessauer and Cole, 1989; Taylor et al., 2003a), and patterns of morphological variation (Parker, 1979; Walker et al., 1997; Taylor et al., 2003a,b). A variety of protein electrophoretic studies identify A. tesselata as a product of hybridization between Aspidoscelis marmorata and Aspidoscelis septemvittata (Neaves, 1969; Parker and Selander, 1976; Dessauer and Cole, 1989; Dessauer et al., 1996), and A. marmorata was identified as the maternal progenitor from restriction fragmentlength polymorphisms of mitochondrial DNA 2
Corresponding Author.
(Densmore et al., 1989a). Histocompatibility of reciprocal skin transplants between individuals of different pattern classes in allopatric (Maslin, 1967) and sympatric associations (Cordes and Walker, 2003) indicate that A. tesselata originated from a single, parthenogenetically capable, F1 female. This evidence of singular origin, together with evidence that color pattern is inherited in a clonal pattern (Dessauer and Cole, 1986; Taylor et al., 2001, 2003a), implicate postformational divergence as the basis for the phenotypic differences within A. tesselata. A geographically restricted example of postformational divergence in A. tesselata concerns the three pattern classes at Sumner Lake, De Baca County, New Mexico (Taylor et al., 1997). Each pattern class, herein designated Sumner C, Sumner D, and Sumner E, is distinguishable by color pattern differences (Taylor et al., 1996, 1997; Walker et al., 1997). The impetus for the present study was the paradox between evidence that A. tesselata originated from a single hybrid individual and the striking morphological and life-history differences between Sumner C and Sumner E. Therefore, one purpose of this study was to use histocompatibility experiments to test the possibility that Sumner C and Sumner E were
POSTFORMATIONAL EVOLUTION IN ASPIDOSCELIS TESSELATA products of separate hybridization events. A second purpose was to more fully describe lifehistory and morphological differences between Sumner C and Sumner E. Finally, we illustrate two disparate results from application of the evolutionary species concept (ESC) to postformational evolutionary divergence in parthenogenetic Aspidoscelis. MATERIALS AND METHODS For skin-grafting experiments, body size of each lizard was used to determine size of the plastic box (29 3 17 3 12 cm or 34 3 29 3 17 cm) in which it was maintained. Each box had 3–5 cm of sand, an ExoTera faux-rock ‘‘Hiding Cave’’ shelter (18 3 15 3 7 cm or 24 3 15 3 7 cm), fallen oak leaves, and a charcoal fiberglass insect-screen covering. Optimal temperature and light conditions required full-spectrum daylight fluorescent lamps with emissions ranging from 33–15% UVA and from 8–2% UVB along with incandescent daylight blue lamps for heat and additional UVA to provide a seasonally adjusted 9–10 h-light interval each day. Daily temperatures in the containers ranged from 298C–368C during the light period and from 228C–288C during the dark period. The lizards were fed yellow mealworms and crickets dusted with vitamin-mineral supplement, and water was provided daily. All SSAR guidelines for ethical treatment of animals and applicable IACUC regulations were followed. Skin-grafting was performed by JEC. One xenograft exchange involved an individual of A. tesselata E and an individual tentatively identified as either Aspidoscelis neomexicana (a parthenogenetic species derived from an Aspidoscelis tigris 3 Aspidoscelis inornata hybridization; Cole et al., 1988) or an Aspidoscelis neomexicana 3 Aspidoscelis sexlineata viridis hybrid. Also, seven reciprocal allografts were exchanged among the five individuals of A. tesselata from Sumner Lake and the two lizards of this species from Fort Sumner (Appendix 1). Before surgery, lizards were immobilized by placing them on a glass pane covering a tray of ice (Cuellar, 1976, 1977; Abuhteba et al., 2000). Skin-grafting was carried out with sterilized surgical instruments under a vertical laminar flow hood with two Sankyo Denki 615T8 germicidal ultraviolet lamps. In each graft exchange, a Miltex dermal biopsy punch sterilized with 100% ethanol was used to cut a circular 3-mm diameter skin patch from the dorsal surface of each lizard. In each experiment, skin patches were exchanged between two lizards to wound sites that had been perfused with 0.9% sterilized saline (autoclaved for 10 min) after removal of the original patch. Each skin graft was covered with a 1 3 1 cm precut strip of TegadermTM dressing.
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Our interpretation of skin-grafting experiments was based on the prediction that lizards tracing their ancestry to the same hybrid individual should be histocompatible among themselves and histoincompatible with members of other such groups. This prediction is supported by observations that although inferred mutations in a parthenogenetic group are potentially capable of affecting the immune responses of individuals (e.g., in , 5% of Aspidoscelis laredoensis A tested; Abuhteba et al., 2000), the proportion of these individuals is not sufficient to mimic graft rejection responses seen between groups of Aspidoscelis derived from different hybrid zygotes (e.g., between 100% of the A. laredoensis A and clonal complex B tested; Abuhteba et al., 2000). Other than specimens collected in 2003 for skin transplant experiments, samples used for lifehistory and morphological comparisons (66 specimens of Sumner C, 59 of Sumner E, and five of Sumner D) included individuals collected as encountered in 1995–1997, and 2002 (Appendix 1). Each specimen was scored for 10 meristic characters (Table 1), and snout–vent length (SVL) was measured with digital calipers to the nearest milimeter from tip of snout to posterior margin of the preanal scales. The small sample of Sumner D (N 5 5) comprised all specimens encountered in 1995, 1996, and 1997; none was seen in 2002 and 2003. Insufficient numbers of mature individuals of Sumner D precluded its inclusion in lifehistory comparisons. Clutch size was estimated from numbers of yolking ovarian follicles 3 mm in diameter and numbers of oviductal eggs, both revealed by dissection of preserved specimens. Length and width of each oviductal egg (Sumner C, N 5 80; Sumner E, N 5 70) was measured to the nearest 0.1 mm with digital calipers. Oviductal egg volume was calculated using the formula for a prolate spheroid: V 5 4/3p (egg length/2) ([egg width/2]2) (Vitt and Breitenbach, 1993). Three meristic color pattern characters (see Table 1), L-breaks, DL-breaks, and PV-breaks undergo ontogenetic changes in A. tesselata (Taylor et al., 2003a). Therefore, we regressed each character on a decreasing sequence of snout–vent lengths to determine the size at which the relationship between character and SVL became nonsignificant, thereby determining the smallest individuals to include in subsamples for statistical tests and procedures. Although our sample of Sumner D did not exhibit a relationship between any of these characters and SVL (P . 0.08), it was necessary to exclude specimens , 73 mm SVL in samples of Sumner C and Sumner E to remove ontogenetic effects. Although this size restriction was applied to all samples used in morphological analyses, even small individuals could be assigned to
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pattern class based on a visual assessment of color pattern features. We used one-way analysis of variance (ANOVA) and t-tests to assess differences among and between sample means. The Tukey HSD post hoc test was used to identify specific differences when ANOVA indicated significant differences among samples. T-tests adjusted for unequal sample variances were used when appropriate. Because all individuals of Sumner C producing six-egg clutches had the same SVL, a one-sample t-test was used to test SVL differences between Sumner C and Sumner E with clutches of this size. Snout–vent length distributions were compared with the Mann-Whitney test. Results of all statistical tests were interpreted based on a 5 0.05. Two multivariate statistical analyses were used to depict the pattern of evolutionary divergence among Sumner C, Sumner D, and Sumner E. Morphological similarities and differences among the three pattern classes were determined by CVA, using pattern classes pooled across four years as a priori groups (44 Sumner C, 41 Sumner E, and 5 Sumner D). To ensure that important characters were not excluded from the CVA model, stepwise character selection was based on F-probabilities of 0.15 for entry and removal (Costanza and Afifi, 1979). Prior probabilities for classifying specimens to group were determined from sample sizes because of the disproportionately small size of the Sumner D sample. A few individuals of Sumner C and Sumner E had been previously misidentified as belonging to the other pattern class (identified in Taylor et al., 2003a). Therefore, we used a principal components analysis (PCA) to verify that individuals had been assigned to the correct a priori groups in the CVA. The PCA, based on a correlation matrix, allowed visualization of meristic variation independent of prior pattern class assignments.
TABLE 1. Meristic characters (and SVL) used in analyses of morphological variation among three syntopic color pattern classes of Aspidoscelis tesselata from the vicinity of Sumner Lake State Park, De Baca County, New Mexico.
RESULTS Fieldwork in five different years revealed no differences among pattern classes in activity periods or habitats used. Therefore, our working assumption has been that phenotypic differences among color pattern classes were not based on epigenetic effects of different environments. Hatchlings have a basic dorsal color pattern consisting of three pairs of white, gray, or graytan longitudinal stripes that subdivide the dorsum into intervening dark fields. Dark fields may contain or develop spots, bars, and vertebral line(s). Collectively, these features define individual pattern classes throughout ontogeny (Walker et al., 1997). Although Sumner D is distinguished by a pair of lines (typically broken or disrupted) in the black to black-brown vertebral field,
SDL-T4
Character abbreviations
GAB
COS LSG
FP GS
PSC L-breaks DL-breaks PV-breaks
SVL
Description
Number of granular dorsal scales in a single row around midbody. There are eight longitudinal rows of enlarged scales making up the ventral body surface. The third ventral row on either side of the midsagittal line terminates anteriorly in the axillary region. The 15th ventral scale posterior to this terminus established the point for beginning the GAB count. Bilateral total of circumorbital scales as standardized by Wright and Lowe (1967). Sum of lateral supraocular granules on both sides of the head. These granular scales are located between the supraoculars and superciliary scales, and the count includes all scales anterior to the suture line between the third and fourth supraoculars. Sum of femoral pores on both thighs. Number of granular gular scales bordering the medial edges of the eight anterior sublabials and the posterior mental. Sum of all scales, including occipitals, contacting the outer perimeter of parietal and interparietal scales. The total number of interruptions by black pigment of the lateral pale stripes. The total number of interruptions by black pigment of the dorsolateral pale stripes. The total number of interruptions by black pigment of the paravertebral pale stripes. Number of sudigital lamellae on the fourth toe of one foot (right was chosen unless damaged). Length of body from tip of snout to posterior edge of preanal scales (in millimeter).
individuals of Sumner C have a single intact or nearly intact zigzagged line. This line has intermittent longitudinal divisions in some individuals, thereby producing a chainlike configuration that resembles the doubled vertebral lines in Sumner D (Taylor et al., 2003a: fig. 8). Sumner E also expresses color pattern variation. At one extreme, the dorsum is dominated by coarse, transverse expansions of dark field areas
POSTFORMATIONAL EVOLUTION IN ASPIDOSCELIS TESSELATA
FIG. 1. Photographic evidence of histocompatibility between living individuals of Aspidoscelis tesselata pattern classes E (west side of Sumner Lake) and C (east side of Sumner Lake). Upper: (A) Allograft hosted by Sumner E (RU 0083) from a Sumner C (RU 0079); lower: (B and C) allografts hosted by a sumner C (RU 0079) from two representatives of Sumner E (RU 0083 and 0081, respectively).
across the stripes. At the other extreme, the dorsum is dominated by prominent stripes, thereby more closely resembling Sumner C (Taylor et al, 2003a: fig, 12). These individuals can be distinguished from Sumner C by the relative number of dark bars disrupting the continuity of the lateral stripe—few breaks in Sumner C and many breaks in Sumner E (Taylor et al., 2003a: fig. 12). Skin Transplant Experiments.—Evidence of the adaptability of the three individuals of Sumner C to a laboratory setting has included their ongoing voracious appetites for mealworms and crickets, excellent physical conditions (Fig. 1), and tolerance of the preparatory regimens and 3 mm wounds involved in each graft exchange. Presently, two of the three Sumner C lizards have been maintained in captivity without noticeable loss of vigor for . 403 days and continue to be used in other experiments. Although they were maintained in the laboratory under similar conditions, one of the two E lizards from the west side of Sumner Lake (RU 0081) and the two from Fort Sumner (GJM 0502, 0529) adapted less well to captivity and experimentation than the Sumner C lizards. They were fitful in their acceptance of food, and deterioration to poor physical condition and early death occurred, in
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part, because of their use in 2–3 reciprocal graft exchanges. The second E lizard from Sumner Lake (Fig. 1, RU 0083), which was used in only one reciprocal graft exchange, matched the three Sumner C lizards in adaptability to cage life; it was sacrificed while in good condition. The maintenance difficulties associated with three of the E lizards did not compromise acceptance of seven of the eight skin grafts attached to E lizards (one graft was lost accidentally eight days after surgery). We were able to maintain the four E lizards in the laboratory for an average of only 291.3 (252–318) days as compared to the much longer period for the Sumner C lizards, two of which remain in robust condition. One exchange of xenografts was made on 27 December 2003 between an individual of pattern class E (GM 0529) and one individual of either A. neomexicana or A. neomexicana 3 A. sexlineata viridis (GM 0534, identity under study) from Fort Sumner. This experiment tested for an immune response capable of rejecting tissue suspected of harboring alien antigens in the A. tesselata from the De Baca County study area. These reciprocal xenografts were quickly rejected and, in both GM 0529 and 0534, rejection was followed by a healing response that closed the wound site. This experiment verified that De Baca County A. tesselata will reject skin grafts from congeners of other historical groups (i.e., species and/or their hybrids) as has been shown for other local groups of this species (Maslin, 1967; Cordes and Walker, 2003). Fieldwork between 1995 and 2003 revealed that pattern class E is the numerically dominant form of A. tesselata on the west side of Sumner Lake (WSL), that both C and E are well represented on the east side of the lake (ESL) and that only E lizards occur at Fort Sumner (FS) about 16 km S of the lake. Three reciprocal allograft exchanges involving ESL C $ WSL E established that these pattern classes, as known from Sumner Lake, are mutually histocompatible. The three grafts transplanted to the two Sumner C lizards (RU 0079, 0080) quickly healed in place without noticeable consequences to either animal (Fig. 1). These grafts have remained viable for 235–245 days at this writing, Three grafts transplanted to the two E lizards also healed into place concurrent with the slow deterioration of RU 0081 and maintenance of robust condition in RU 0083 (Fig. 1). These grafts remained viable and firmly attached at the wound sites for 148–158 days until the deaths of the lizards (Table 2). All other combinations of allograft exchanges involving Sumner Lake and Fort Sumner individuals of A. tesselata also demonstrated mutual histocompatibility (Table 2) and genetic homogeneity in gene complexes affecting immune responses.
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TABLE 2. Skin transplant regimens for three individuals of Aspidoscelis tesselata C from east side of Summer Lake (ESL, RU 0079, 0080, 0082) and two A. tesselata E from west side of Sumner Lake (WSL, RU 0081, 0083) and two from Fort Sumner (FS, GJM 502, 529), De Baca County, New Mexico. Left to right: site of collection, (museum number of lizard and pattern class), days graft retained, $, days graft retained, (museum number of lizard and pattern class), site of collection, (date of graft exchange)
ESL ESL ESL ESL ESL WSL WSL a
(0079 (0079 (0080 (0080 (0082 (0081 (0081
C) C) C) C) C) E) E)
235 245 242 317 242 319 235
$ $ $ $ $ $ $
148 158 155 144 88 165 8a
(0081 (0083 (0081 (0529 (0502 (0502 (0080
E) E) E) E) E) E) C)
WSL WSL WSL FS FS FS ESL
(01/03/04) (12/24/03) (12/27/03) (10/11/03) (12/27/03) (10/11/03) (12/27/03)
Accidentally lost.
SVL of Gravid Females and Clutch Size.— Sumner C (N 5 40; mean 6 SE: 93.7 6 0.46; 4.4 6 0.16) and Sumner E (N 5 42; 84.8 6 0.86; 3.4 6 0.17) differed significantly in both SVL of gravid females and clutch size (t62.330 5 9.141, P , 0.0005 and t80 5 4.309, P , 0.0005, respectively). Some individuals produce two clutches in the same year as evidenced by the simultaneous presence of yolking ovarian follicles 3 mm and corpora lutea. This was true for both pattern classes in 1996 and 1997 and for Sumner E in 2002. Relationship between Clutch Size and SVL.—A positive relationship between clutch size and SVL was evident in both Sumner E (R2 5 0.55; F1,40 5 49.416, P , 0.0005) and Sumner C (R2 5 0.20; F1,38 5 9.494, P 5 0.004). Coefficients of determination (R2) and F-ratios identify Sumner E as having the stronger relationship between the two variables. SVL Frequency Distributions.—Sumner C and Sumner E were significantly different in body length distributions (Fig. 2). This was true both for gravid females (40 Sumner C, 46 Sumner E: Mann-Whitney U 5 1724.0, P , 0.0005) and for all individuals in the samples (67 Sumner C, 62 Sumner E: Mann-Whitney U 5 2765.5, P 5 0.001). Snout–vent length distributions for complete samples are bimodal because of a typical size-gap between sexually immature and reproductively mature individuals. This two-group pattern was pronounced in Sumner C but less distinct in Sumner E because of several small reproductively mature individuals associated with the juvenile class. Reproduction at a smaller size increased the proportion of gravid individuals in Sumner E: 46 of 62 Sumner E individuals (74%) were gravid compared to 40 of 67 Sumner C individuals (60%; Fig. 2). Basis of SVL—Clutch Size Differences.—On average, Sumner C had larger gravid individu-
FIG. 2. Body size (SVL) distributions and reproductive status of females in samples of Sumner C and Sumner E of Aspidoscelis tesselata from Sumner Lake State Park, De Baca County, New Mexico.
als. This might be a reflection of its greater longevity or different growth rates between the two pattern classes (Taylor et al., 1997). Recently hatched individuals of both pattern classes have similar SVLs (Taylor et al., 1997), and similar oviductal egg volumes reinforce this observation. In contrast to clutch size, egg volume was not related to SVL in either pattern class (Sumner C: R2 5 0.001, P 5 0.77; Sumner E: R2 5 0.008, P 5 0.46). Therefore, although SVL differed significantly between Sumner C and Sumner E for each clutch-size class, there were no significant differences between the two-pattern classes in egg volume (Table 3). A faster rate of posthatching growth in Sumner C could explain its larger mean SVL and clutch size. If growth rates differ, this should manifest itself in the size distributions of smaller individuals in the two samples. Although a few reproductively mature individuals of Sumner E were included (Fig. 2), we selected individuals , 75 mm SVL for testing because this size restriction maintained normal distributions (Shapiro-Wilk statistic: Sumner C: 0.924, 25 df, P 5 0.06; Sumner E: 0.966, 19 df, P 5 0.70) and homogeneous variances (Levene statistic 5 2.652; 1,42 df; P 5 0.11) between the two subsamples. For individuals , 75 mm SVL, Sumner C was larger (69.8 6 0.62, 64–74 mm, N 5 25) than Sumner E (65.4 6 1.11, 54–73 mm, N 5 19; t42 5 3.735, P 5 0.001), and the SVL distributions of these subsamples were also different (MannWhitney U 5 106.0, P 5 0.002). Distributional Differences.—The relative numbers of Sumner C and Sumner E differed between the sampling sites on the East side of Sumner Lake (C 5 63, E 5 45) and the West sides of Sumner Lake and Pecos River below the dam (C 5 3, E 5 14; v2 5 9.756, P 5 0.002). This may
POSTFORMATIONAL EVOLUTION IN ASPIDOSCELIS TESSELATA
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TABLE 3. Comparisons of SVL of gravid females and egg volume between color pattern classes C and E from Sumner Lake State Park, De Baca County, New Mexico. Mean 6 1 SE, (range limits), and sample size are shown. All SVL comparisons (in millimeter) were significantly different, and none of the egg volume comparisons (in cubic centimeter) was significantly different at a 5 0.05. Pattern class Clutch size
Attribute
3
SVL Egg volume SVL Egg volume SVL Egg volume SVL Egg volume
4 5 6
Sumner C
93.0 6 0.58 0.74 6 0.051 91.2 6 0.77 0.70 6 0.029 95.3 6 0.34 0.73 6 0.02 98.0 0.65 6 0.053
Sumner E
(91–95), 9 (0.58–1.00), (88–97), 20 (0.46–1.08), (92–98), 45 (0.50–1.06), (98–98), 6 (0.42–0.78),
be related to impediments to dispersal from eastern source groups, but the exact cause of the numerical asymmetry is unknown. However, relative numbers of Sumner C and Sumner E were not significantly different in either composite samples from both sides of the lake (C 5 66, E 5 59; v2 5 0.392, P 5 0.531) or in the east-side samples (C 5 63, E 5 45; v2 5 3.000, P 5 0.083). Morphological Variation.—Stepwise selection of meristic characters from 10 candidate variables (Table 4) indicated that discrimination could be achieved with two of the 10 characters, L-breaks and GAB. The CVA model correctly classified all specimens of Sumner C and Sumner E to a priori groups. In contrast, all five individuals of Sumner D were misclassified as belonging to the Sumner C group. Correspondingly, Sumner C and Sumner E lizards showed pronounced morphological differences, whereas such differences were lacking between Sumner C and Sumner D (Fig. 3A). This same evolutionary pattern, Sumner D meristically indistinguishable from Sumner C and the morphological segregation of these two
82.2 6 0.84 0.66 6 0.024 86.2 6 0.59 0.70 6 0.027 91.0 6 0.33 0.72 6 0.062 90.5 6 0.15 0.62 6 0.037
9 20 45 6
(75–89), 24 (0.41–0.87), (83–92), 24 (0.42–1.00), (90–92), 10 (0.40–1.04), (90–91), 12 (0.47–0.89),
24 24 10 12
groups from Sumner E, was expressed by a PCA (Fig. 3B). DISCUSSION An example of major postformational divergence in a parthenogenetic species involves two of the three pattern classes of A. tesselata at Sumner Lake. Our results from reciprocal allograft exchanges involving three individuals of pattern class C and four of pattern class E from Sumner Lake and Fort Sumner, De Baca County, New Mexico, demonstrated mutual histocompatibility. This level of homogeneity for control of immune responses to skin allografts is consistent with a hypothesis that these and other pattern classes of A. tesselata were subsequently derived from genetic changes (i.e., mutation or recombination) among the descendants of one parthenogenetically capable hybrid individual of A. marmorata 3 A. septemvittata (also see Maslin, 1967; Cordes and Walker, 2003). Major differences between Sumner C and Sumner E include alternative adaptations for maximizing fitness. On average, reproductively
TABLE 4. Comparisons of 10 meristic characters among three syntopic color pattern classes of Aspidoscelis tesselata from Sumner Lake State Park, De Baca County, New Mexico. Mean 6 1 SE, (range limits), and sample size are shown. Means bound together by an underline are not significantly different at a 5 0.05. Statistics based on individuals .72 mm SVL in Sumner C and Sumner E. Pattern class Character
L-breaks DL-breaks PV-breaks GAB COS FP LSG SDL-T4 GS PSC
Sumner C
4.3 1.5 4.5 91.7 16.4 41.1 39.5 36.5 24.0 20.9
6 6 6 6 6 6 6 6 6 6
0.36 (0–12), 44 0.16 (0–6), 44 0.35 (0–11), 44 0.46 (86–99), 44 0.37 (13–25), 44 0.22 (37–44), 44 0.58 (33–50), 44 0.20 (34–40), 44 1.11 (17–37), 44 0.22 (18–24), 44
Sumner D
3.0 1.8 5.0 91.4 17.4 41.2 41.2 36.2 20.6 20.2
6 6 6 6 6 6 6 6 6 6
0.71 0.20 1.05 0.93 0.68 0.74 1.93 0.37 0.51 0.49
(1–5), 5 (1–2), 5 (3–9), 5 (89–94), (15–19), (39–43), (36–48), (35–37), (19–22), (19–21),
Sumner E
5 5 5 5 5 5 5
22.2 11.4 14.0 98.4 19.1 42.3 37.7 36.7 25.2 20.2
6 6 6 6 6 6 6 6 6 6
0.64 0.80 0.89 0.53 0.23 0.27 0.86 0.17 1.07 0.49
(13–31), 42 (3–23), 41 (5–25), 41 (91–109), 43 (15–24), 43 (39–46), 43 (26–53), 43 (35–39), 43 (19–39), 43 (19–21), 43
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mature individuals of Sumner C are significantly larger than those of Sumner E; therefore, because of the positive relationship between clutch size and SVL, Sumner C produces a larger mean clutch. By reproducing at a smaller size, a greater proportion of Sumner E can be gravid in each reproductive season, but there could be a cost. Because adult survival is inversely related to age of reproductive maturity (Shine and Charnov, 1992), Sumner E might have a shorter mean lifespan. Nevertheless, similar numbers of Sumner E and Sumner C on the east side of Sumner Lake suggest that the trade-off between reproducing at a smaller size and the smaller clutches (and perhaps shorter live spans) that result is presently effective in maintaining pattern class E at this locality. These life-history differences between Sumner C and Sumner E are as different as those between syntopic groups of Aspidoscelis exsanguis and Aspidoscelis flagellicauda (Taylor and Caraveo, 2003), two species originating from hybridization events between different sets of progenitor species with unresolved taxonomies (Good and Wright, 1984; Densmore et al., 1989b; Reeder et al., 2002). Our current samples provide a correction to the observation that Sumner E, but not Sumner C, exhibits a relationship between clutch size and SVL (Taylor et al., 1997). Sumner C also exhibits this relationship, but it is weaker than in Sumner E. Persistence of life-history and morphological differences between Sumner C and Sumner E in a shared environment is evidence that epigenetic factors are not responsible for their differences, and histocompatibility between them substantiates that genetic differences were acquired subsequent to a single hybridization event. Based on the magnitude of the phenotypic gaps between Sumner C and Sumner E, it seems likely that divergent characteristics were present in the colonists of the Sumner Lake locality rather than originating in situ, thereby providing a contrast to the likely mutational origin of Sumner D from Sumner C at this locality (Taylor et al., 2003a). That all disjunct groups of pattern class D are of recent origin is supported by their close morphological and life history resemblance to a sympatric, progenitor pattern class (Taylor et al., 1996, 1999a,b, 2000, 2003a, 2005). Since the phenotypic differences between Sumner C and Sumner E reflect separate evolutionary trajectories (i.e., biologically, they are functioning as different species in the field), can either entity be accommodated as a species under the ESC? There are two fundamental philosophical positions regarding the taxonomic treatment of parthenogenetic vertebrates: either parthenogenetic entities are not recognized formally (summarized in Dawley, 1989), or they are included in the Linnaean nomenclatural system
FIG. 3. Depiction of multivariate morphological variation among three color pattern classes of Aspidoscelis tesselata from Sumner Lake State Park, De Baca County, New Mexico. Axis percentage refers to the proportion of sample variation explained by that axis. (A) Discrimination among groups using a canonical variate analysis of two meristic characters, L-breaks and GAB. (B) Principal components analysis using a correlation matrix of six meristic charaters in which there were significant differences among at least two of the three color pattern classes (L-breaks, DL-breaks, PV-breaks, GAB, COS, and FP).
(Frost and Wright, 1988; Frost and Hillis, 1990; Reeder et al., 2002). For the latter approach, unisexual organisms are accommodated by a number of species concepts: the phylogenetic species concept of Wheeler and Platnick (2000), the phylogenetic species concept of Mishler and Theriot (2000), the evolutionary species concept of
POSTFORMATIONAL EVOLUTION IN ASPIDOSCELIS TESSELATA Wiley and Mayden (2000), and the non-Mendelian species concepts of Cole (1985), Frost and Wright (1988), and Echelle (1990). Neither of the two phylogenetic species concepts is particularly useful for reconstructing species-level evolutionary history in Aspidoscelis because of the general scarcity of derived character states in morphological characters (see Grismer 1999; Walker et al., 2001; Reeder et al., 2002). Furthermore, in contrast to the viewpoint of Echelle (1990), which is compatible with the evolutionary species concept (ESC), the uniparental species concepts of Cole (1985) and Frost and Wright (1988) do not recognize postformational evolution as a speciation mechanism in parthenogenetic vertebrates. Therefore, we consider the applicability of the ESC to two well-studied examples of postformational divergence in parthenogenetic Aspidoscelis. According to Wiley and Mayden (2000), ‘‘An evolutionary species is an entity composed of organisms that maintains its identity from other such entities through time and over space and that has its own independent evolutionary fate and historical tendencies.’’ A potential problem inherent in this concept is the opportunity for overreductionism, particularly in unisexual groups capable of clonal perpetuation of all degrees of diagnosable variation—molecular to morphological (Cole, 1985, 1990). Therefore, the conservative approach for demarcating parthenogenetic species uses individual hybridization events to mark their monophyletic legitimacy (Frost and Wright, 1988; Frost and Hillis, 1990). In keeping with the long history of disagreement among investigators of this genus, even this philosophically satisfying operationalism is not free of controversy. For example, different taxonomies could be advocated depending on the perception of what originates, in the way of parthenogenetic entities, from multiple hybridization events between the same two progenitor species (either same or different pairs of individuals, either same or different egg clutches). In one case, parthenogenetic entities originating from several fertilizations between the same parental species could be viewed as representing the same species, irrespective of the time interval between such events (Cole, 1985, 1990). In contrast, parthenogens originating from multiple fertilizations between the same parental species could be viewed as representing multiple species, each marked by an independent origin, even if derived from the same clutch of eggs (Frost and Wright, 1988; Frost and Hillis, 1990). Both of these positions reject the formal recognition of entities originating by clonal divergence subsequent to a basal origin from hybridization (Echelle, 1990). However, there are such entities, some of which are as biologically distinctive as those originating from independent hybridization events. Because
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these postformational groups are products of evolution, their candidacy for formal recognition should be examined rather than ignored. One example involves Aspidoscelis maslini and Aspidoscelis cozumela from the Yucata´n Peninsula. Prior to 1995, these were treated as subspecies, with maslini considered a subspecies of cozumela (Fritts, 1969; Moritz et al, 1992). This arrangement is inappropriate for two reasons. Fundamentally, karyotypic evidence shows that cozumela is a mutational derivative of maslini (ManriquezMoran et al., 2000). Therefore, knowledge of this ancestor-descendant relationship is obliterated if maslini is depicted as an intraspecific variant of cozumela. Second, relegating maslini to A. cozumela obscures its individuality. Aspidoscelis maslini and A. cozumela, both traceable to the same hybridization event (Aspidoscelis angusticeps 3 Aspidoscelis deppii), show morphological divergence similar to the level exhibited by A. cozumela and Aspidoscelis rodecki, entities traceable to two separate hybridization events between A. angusticeps and A. deppii (Fritts, 1969; Moritz et al., 1992; Hernandez-Gallegos et al., 1998, 2003). Taylor and Cooley (1995a, b) used this equivalency of morphological differences, and a fresh perspective of postformational evolution in parthenogenetic entities (Echelle, 1990), to recommend species rank for maslini, a proposal that was rejected by Hernandez-Gallegos et al. (1998) because of histocompatibility between maslini and cozumela. However, species rank for maslini was recommended by Manriquez-Moran et al. (2000) based on a karyotypic reconstruction of their origins. Aspidoscelis maslini has a karyotype (2n 5 47) comprising haploid sets of chromosomes from each of the two progenitor species (22 from A. angusticeps and 25 from A. deppii). In contrast, A. cozumela has a karyotype (2n 5 50) consistent with clonal perpetuation of chromosomes derived from three centric fissions originating in A. maslini. Therefore, A. cozumela originated from an individual of A. maslini, an event marked by a substantial karyotypic change (Reeder et al., 2002). The derivation of cozumela from maslini represents the disruption of a preexisting tokogenetic system and the establishment of a new system that Wiley and Mayden (2000) equate to speciation. Because A. maslini originated from one parthenogenetic hybrid (Moritz et al., 1992; Hernandez-Gallegos et al., 1998), the phenotypic differences between histocompatible maslini and cozumela can be ascribed to postformational mutations marked by the derived karyotype of cozumela. Another example of formal recognition of postformational groups involves parthenogenetic Lacerta sapphirina and Lacerta bendimahiensis (Jinzhong et al., 2000). Because of their allopatric distributions (A. maslini on the mainland, A. cozumela on Isla
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Cozumel), the elevation of maslini (described and diagnosed by Fritts, 1969) to species rank is uncomplicated. Using the evolutionary species concepts of Frost and Hillis (1990 [as applied to bisexual species]) and Wiley and Mayden (2000), shifting maslini from subspecies to species rank is no more controversial than shifting bisexual entities from subspecies to species rank. Although the ESC inherently lacks operational guidelines, diagnosability of allopatric populations has been used as justification for elevating a number of bisexual subspecies to species rank (Collins, 1991), an action justified by Collins (1992) and endorsed by Frost et al. (1992), following challenges by Montanucci (1992) and Van Devender et al. (1992). Although species cohesion theoretically involves mating bonds in bisexuals and ecological constraints in unisexuals, species decisions made under the ESC should carry the same risk of error for both uniparental and bisexual entities. In addition to life-history differences between Sumner C and Sumner E, there is a clear pattern of morphological divergence in which the distinctiveness of Sumner E contrasts with the remarkable similarity between Sumner C and Sumner D. The name tesselata is indirectly associated with pattern class C through the neotype of A. tesselata, a representative of pattern class Colorado D. Because Colorado D is a likely postformational derivative of pattern class C (Taylor et al., 1996, 1999a, 2000), the focus of possible formal recognition shifts to Sumner E. However, unlike the diagnosability of continental A. maslini and insular A. cozumela, there are confounding mosaic patterns of allozyme, karyotypic, morphological, and life history variation among disjunct groups of pattern class E (Taylor et al., 2000, 2003a). Therefore, maintaining identity over space, a condition of the ESC, is not met in this example. Although asynchronous evolution of phenotypic characters is expected from random mutations in clonally reproducing species, this also guarantees that the taxonomic treatment of postformational divergent groups will be uneven as well. This problem is not unique to parthenogenetic entities, and the effectiveness of matching species-level taxonomy to evolutionary history includes factors such as the geographic relationships of divergent groups within each reproductive mode. Two situations can be anticipated when applying the ESC to postformational evolution in parthenogenetic Aspidoscelis. In one, illustrated by A. maslini and A. cozumela, allopatric distributions of diagnosable entities facilitate their formal recognition. However, unlike the geographically restricted distributions of A. cozumela and A. rodecki, several geographically scattered, isolated groups of A. maslini have been found.
Nevertheless, their collective meristic variation is no greater than that exhibited within the geographically restricted A. cozumela and A. rodecki (Taylor and Cooley, 1995a), and their color pattern diagnosability holds up across their range. In contrast, the pattern of morphological variation in A. tesselata, also comprising scattered, isolated groups, is a complex geographic mosaic of color pattern and meristic similarities and differences, thereby compromising the diagnosability of entities such as Sumner E (Taylor et al., 2003a). The inevitable arbitrariness associated with decisions on what constitutes major and minor clonal divergence suggests that A. tesselata, as presently understood, is best perceived as a single, highly variable parthenogenetic species. This perception will probably obtain for most parthenogenetic Aspidoscelis that exhibit postformational divergence. However, Aspidoscelis dixoni (Scudday, 1973), a species sharing a hybridization event with A. tesselata (Cordes and Walker, in press), also comprises divergent postformational groups, one of which is accommodated by the ESC for formal taxonomic recognition (Walker et al., 1994). Acknowledgments.—We express our appreciation to the State of New Mexico, Department of Game and Fish, for Scientific Collecting Permits (1905 issued to HLT and 1850 issued to JEC), and to K. Taylor for assistance in the field in 1995. We are grateful to R. Terrell for his interest in this study and for providing Special Use Permits and hospitality at Sumner Lake State Park. Summer Research Grants from TSSC and SPARC committees at Regis University supported field work of HLT. LITERATURE CITED ABUHTEBA, R. M., J. M. WALKER, AND J. E. CORDES. 2000. Genetic homogeneity based on skin histocompatibility and the evolution and systematics of parthenogenetic Cnemidophorus laredoensis (Sauria: Teiidae). Canadian Journal of Zoology 78:895–904. COLE, C. J. 1985. Taxonomy of parthenogenetic species of hybrid origin. Systematic Zoology 34:359–363. ———. 1990. When is an individual not a species? Herpetologica 46:104–108. COLE, C. J., H. C. DESSAUER, AND G. F. BARROWCLOUGH. 1988. Hybrid origin of a unisexual species of whiptail lizard, Cnemidophorus neomexicanus, in western North America: new evidence and a review. American Museum Novitates 2905:1–38. COLLINS, J. T. 1991. Viewpoint: a new taxonomic arrangement for some North American amphibians and reptiles. Herpetological Review 22:42–43. ———. 1992. The evolutionary species concept: a reply to Van Devender et al. and Montanucci. Herpetological Review 23:43–46. CORDES, J. E., AND J. M. WALKER. 2003. Skin histocompatibility between syntopic pattern classes C and D
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TAYLOR, H. L., AND Y. CARAVEO. 2003. Comparison of life history characteristics among syntopic assemblages of parthenogenetic species: two color pattern classes of Aspidoscelis tesselata, A. exsanguis, A. flagellicauda, and three color pattern classes of A. sonorae (Squamata: Teiidae). Southwestern Naturalist 48:685–692. TAYLOR, H. L., AND C. R. COOLEY. 1995a. A multivariate analysis of morphological variation among parthenogenetic teiid lizards of the Cnemidophorus cozumela complex. Herpetologica 51:67–76. ———. 1995b. Patterns of meristic variation among parthenogenetic teiid lizards (genus Cnemidophorus) of the Yucata´n Peninsula and their progenitor species, C. angusticeps and C. deppei. Journal of Herpetology 29:583–592. TAYLOR, H. L., J. M. WALKER, AND J. E. CORDES. 1996. Systematic implications of morphologically distinct populations of parthenogenetic whiptail lizards: Cnemidophorus tesselatus pattern class D. Herpetologica 52:254–262. ———. 1997. Reproductive characteristics and body size in the parthenogenetic teiid lizard Cnemidophorus tesselatus: comparison of sympatric color pattern classes C and E in De Baca County, New Mexico. Copeia 1997:863–868. ———. 1999a. Monthly distributions of size classes and reproductive status in Cnemidophorus tesselatus (Sauria: Teiidae) from southeastern Colorado. Herpetological Review 30:205–207. ———. 1999b. Possible phylogenetic constraint on clutch size in the parthenogenetic teiid lizard Cnemidophorus neotesselatus. Journal of Herpetology 3:319–323. ———. 2000. Ecological patterns of body-size and clutch-size variation in the parthenogenetic teiid lizard Cnemidophorus tesselatus. Herpetologica 56:45–54. TAYLOR, H. L., C. J. COLE, L. M. HARDY, H. C. DESSAUER, C. R. TOWNSEND, J. M. WALKER, AND J. E. CORDES. 2001. Natural hybridization between the teiid lizards Cnemidophorus tesselatus (parthenogenetic) and C. tigris marmoratus (bisexual): assessment of evolutionary alternatives. American Museum Novitates 3345:1–64. TAYLOR, H. L., C. J. COLE, H. C. DESSAUER, AND E. D. PARKER JR. 2003a. Congruent patterns of genetic and morphological variation in the parthenogenetic lizard Aspidoscelis tesselata (Squamata: Teiidae) and the origins of color pattern classes and genotypic clones in eastern New Mexico. American Museum Novitates 3424:1–40. TAYLOR, H. L., J. A. LEMOS-ESPINAL, AND H. M. SMITH. 2003b. Morphological characteristics of a newly discovered population of Aspidoscelis tesselata (Squamata: Teiidae) from Chihuahua, Mexico, the identity of an associated hybrid, and a pattern of geographic variation. Southwestern Naturalist 48:692–700. TAYLOR, H. L., J. M. WALKER, J. E. CORDES, AND G. J. MANNING. 2005. Life history characteristics support recent origins of D-designation color pattern classes in parthenogenetic Aspidoscelis tesselata (Squamata: Teiidae). Southwestern Naturalist 50:258–262. VAN DEVENDER, T. R., C. H. LOWE, H. K. MCCRYSTAL, AND H. E. LAWLER. 1992. Viewpoint: reconsider sug-
gested systematic arrangements for some North American amphibians and reptiles. Herpetological Review 23:10–14. VITT, L. J., AND G. L. BREITENBACH. 1993. Life histories and reproductive tactics among lizards in the genus Cnemidophorus (Sauria: Teiidae). In J. W. Wright and L. J. Vitt (eds.), Biology of Whiptail Lizards (Genus Cnemidophorus), pp. 211–243. Oklahoma Museum of Natural History, Norman. VRIJENHOEK, R. C. 1989. Genetic and ecological constraints on the origins and establishment of unisexual vertebrates. In R. M. Dawley and J. P. Bogart (eds.), Evolution and Ecology of Unisexual Vertebrates, pp. 24–31. New York State Museum Bulletin 466, Albany. WALKER, J. M., J. E. CORDES, C. C. COHN, H. L. TAYLOR, R. V. KILAMBI, AND R. L. MEYER. 1994. life history characteristics of three morphotypes in the parthenogenetic Cnemidophorus dixoni complex (Sauria: Teiidae) in Texas and New Mexico. Texas Journal of Science 46:27–33. WALKER, J. M., J. E. CORDES, AND H. L. TAYLOR. 1997. Parthenogenetic Cnemidophorus tesselatus complex (Sauria: Teiidae): a neotype for diploid C. tesselatus (Say, 1823), redescription of the taxon, and description of a new triploid species. Herpetologica 53:233–259. WALKER, J. M., J. A. LEMOS-ESPINAL, J. E. CORDES, H. L. TAYLOR, AND H. M. SMITH. 2001. Allocation of populations of whiptail lizards to septemvittatus Cope, 1892 (genus Cnemidophorus) in Chihuahua, Mexico, and the scalaris problem. Copeia 2001:747–765. WHEELER, Q. D., AND N. I. PLATNICK. 2000. A critique from the Wheeler and Platnick phylogenetic species concept perspective: problems with alternative concepts of species. In Q. D. Wheeler and R. Meier (eds.), Species Concepts and Phylogenetic Theory: A Debate, pp. 133–145. Columbia Univ. Press, New York. WILEY, E. O., AND R. L. MAYDEN. 2000. The evolutionary species concept. In Q. D. Wheeler and R. Meier (eds.), Species Concepts and Phylogenetic Theory: A Debate, pp. 70–89. Columbia Univ. Press, New York. WRIGHT, J. W., AND C. H. LOWE. 1967. Hybridization in nature between parthenogenetic and bisexual species of whiptail lizards (genus Cnemidophorus). American Museum Novitates 2286:1–36. ZWEIFEL, R. G. 1965. Variation in and distribution of the unisexual lizard, Cnemidophorus tesselatus. American Museum Novitates 2235:1–49. Accepted: 18 February 2005.
APPENDIX 1 Specimens Examined (by locality).—The three adults of Sumner C used in the skin-grafting experiments were captured on the east side of Sumner Lake, De Baca County, New Mexico, by HLT on 19 (RU 0079, 0080) and 20 (RU 0082) July 2003. Two of the E lizards used in the experiments were captured on the west side of Sumner Lake by HLT on 19 (RU 0081) and 20 (RU 0083) July 2003, and two were captured at Fort Sumner, De Baca County, by GJM on 20 June 2003 (GM 0502: along railroad tracks near depot in Fort Sumner) and 22 June 2003 (GM 0529:De Baca County Landfill) during
POSTFORMATIONAL EVOLUTION IN ASPIDOSCELIS TESSELATA a separate expedition. The putative Aspidoscelis neomexicana or A. neomexicana 3 A. sexlineata viridis hybrid (GM 534) was also collected along railroad tracks near the depot in Fort Sumner. RU and GM lizards were transported by auto to Denver and Fayetteville, respectively, and then shipped to JEC in Eunice. Specimens used for morphological and life history components of the study were all collected from Sumner Lake State Park, De Baca County, New Mexico, as follows: Aspidoscelis tesselata, pattern class C: New Mexico, De Baca County, Sumner Lake State Park, Westside Campground area: 14 June 1995 (RU 9507; 7 June 1996 (RU 9651); terrace on west side Pecos River via road south of hwy 203 to West River Picnic area, then on flats north of unimproved road providing access to area to the west: 1 July 1997 (RU 9735); east side of Pecos River and Sumner Lake from arroyo on south side of hwy 203 (southwest of the road to Eastside Campground), along road to Eastside Campground and primitive road east and north 5.0 km into primitive area: 15 June 1995 (RU 9518, 9521); 16 June 1995 (RU 9533-9537, 9539-9541); 2 June 1996 (RU 9602-9604); 3 June 1996 (RU 9608-9611, 9614, 9615); 4 June 1996 (RU 9626, 9627); 5 June 1996 (RU 9629, 9630); 6 June 1996 (RU 9633); 7 June 1996 (RU 9637, 9638, 9640-9642, 9647; 29 June 1997 (RU 9709-9712); 30 June 1997 (RU 97259729); 1 July 1997 (RU 9737-9740); 2 July 1997 (RU 9745, 9746); 3 June 2002 (RU 02025-02031); 5 June 2002 (RU 02037, 02041); 6 June 2002 (RU 02043, 02044); 8 June 2002 (RU 02051); 11 June 2002 (GLM 457, 460-463); 12 June 2002 (GLM 471). Aspidoscelis tesselata, pattern class E: New Mexico, De Baca County, Sumner Lake State Park, Westside Campground area: 14 June 1995 (RU 9508-9516; 15 June 1995 (RU 9519, 9520); 3 June 1996 (RU 9616);
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terrace on west side Pecos River via road south of hwy 203 to West River Picnic area, then on flats north of unimproved road providing access to area to the west: 2 June 1996 (RU 9605); 1 July 1997 (RU 9736); east side of Pecos River and Sumner Lake from arroyo on south side of hwy 203 (southwest of the road to Eastside Campground), then 5.0 km north of hwy 203 along road to Eastside Campground and continuing east and north to primitive area: 15 June 1995 (RU 9522, 9523); 16 June 1995 (RU 9538, 9542, 9543); 2 June 1996 (RU 9601); 3 June 1996 (RU 9613); 4 June 1996 (RU 9625, 9628); 5 June 1996 (RU 9631); 6 June 1996 (RU 9634, 9635); 7 June 1996 (RU 9639, 9643-9646, 9648); 29 June 1997 (RU 97139716); 30 June 1997 (RU 9730-9732); 1 July 1997 (RU 9742-9744); 2 July 1997 (RU 9747-9750); 3 June 2002 (RU 02032-02034); 4 June 2002 (RU 02035, 02036); 5 June 2002 (RU 02038, 02039, 02042); 9 June 2002 (02054); 6 June 2002 (RU 02045, 02046); 11 June 2002 (GLM 458); 12 June 2002 (GLM 469, 474). Aspidoscelis tesselata, pattern class D: New Mexico, De Baca County, Sumner Lake State Park, east side of Pecos River and Sumner Lake from arroyo on south side of hwy 203 (southwest of the road to Eastside Campground), then 5.0 km north of hwy 203 along road to Eastside Campground and continuing east and north to primitive area: RU 9517, 9612, 9632, 9741; terrace on west side Pecos River via road south of hwy 203 to West River Picnic area, then on flats north of unimproved road providing access to area to the west: UADZ 5744. Specimens RU 9507 and 9647 were assigned to pattern class E in Taylor et al. (1997; 2000) but were reassigned to pattern class C by Taylor et al. (2003a). However, neither individual was gravida; thus, clutch size comparisons between Sumner C and Sumner E in Taylor et al. (1997, 2000) are not affected.
