Female fecundity in a hybrid zone between two chromosome races of the Sceloporus grammicus complex (Sauria, Phrynosomatidae).
Studies of Robertsonian heterozygotes have tended to examine reproductive parameters in males. This is largely due to the difficulty in obtaining sufficient meiotic material from females. Sex-related differences are expected in the case of meiotic breakdown (Gropp and Winking 1981; Redi and Capanna 1988). In males, aneuploid spermatocytes often fail to mature into viable gametes and are selected against or degenerate (Stewart-Scott and Bruere 1987). Disruption of spermatogenesis may result in total sterility (Gustavsson et al. 1989) or simply a decrease in gamete viability. Because sperm are produced in excess, decreased viability may not lead to a loss in fecundity. In contrast, the reduced number of total gametes produced by females may increase the likelihood that meiotic disruption produces measurable reductions in fecundity (number and quality of progeny). Increased frequencies of meiotic nondisjunction have been reportedfrom female Robertsonian heterozygotes in humans and Mus (Gropp and Winking 1981; Redi and Capanna 1988; Searle 1988; Garagna et al. 1990). However, Mittwoch et al. (1990) found gametocyte reduction to be less severe in female mice, and some studies reported balanced levels of gametogenesis between the sexes (White et al. 1978). Thus, no general conclusion can be made regarding differential fitness costs of chromosomal heterozygosity to males and females.
Sceloporus grammicus represents an ideal system in which to examine the effects of chromosomal heterozygosity on female reproductive parameters. Females produce one brood each year and are viviparous (Guillette and Casas-Andreu 1980, 1981). Thus, data sets could be collected from both individual females and their offspring during a defined time period. This study was designed to quantify the extent of reproductive failure among females collected within this hybrid zone and to assess the degree to which fecundity reduction is correlated with the level of chromosomal heteroygosity.
MATERIALS AND METHODS
A total of 124 gravid females representing a subset of those examined by Sites el al. (1995) were collected from within and adjacent to the Tulancingo hybrid zone during February 1991. Collection was timed to coincide with the female reproductive cycle such that females would be gravid and near parturition. Reproductive condition of all females was assessed and the number and viability of embryos recorded (embryos were consistently obtained at advanced stages of development, easily fitting the most stringent parity criteria proposed by Blackburn (1993; [ILLUSTRATION FOR FIGURE 1 OMITTED]). Total body length (snoutvent, SVL) of each female was measured within 1 mm.
Karyotypes were prepared for each female as described previously (Reed et al. 1992). For comparative analyses, females were assigned by karyotype to either one of two parental groups (F5 or FM2) or designated as chromosomal intermediates, hereafter referred to as intermediates. Assignment of females to the FM2 group is somewhat tenuous. This group probably includes females heterozygous at both chromosomes 3 and 4 or heterozygous at chromosome 3 and not 4. Chromosomes 3 and 4 are morphologically indistinguishable, and without meiotic pairing data it is not possible to distinguish between various combinations of these chromosomes. The rearrangements of chromosomes 1, 2, and 6 can be unambiguously identified and served as marker chromosomes for the analysis of hybrids.
For comparative purposes, intermediates were further classified by the number of heterozygous marker chromosomes (HM) in the karyotype. Individual markers were assigned a score of 0 if homozygous (AA or BB) and 1 if heterozygous (AB). All heterozygous combinations of chromosome 2 including recombinant morphologies were scored as 1. Thus, HM scores range from 0 to 3. We recognize that grouping of females by HM score neglects some information in the karyotype. For example, HM = 0 females are homozygous at all three markers, yet may be heterozygous at chromosomes 3 and/or 4 (see IBH 7518-5 and BYU 43118 in the Appendix). In addition, this grouping obscures cases in which the markers are homozygous but the female is obviously of mixed parentage (e.g., IBH 7520-4).
Viable progeny (N = 267) from 57 females were processed for karyotypes. Chromosome preparations of embryos were made by grinding a caudal section of the embryo in a hypotonic solution (0.75M KCl) followed by methanol:acetic acid fixation. Chromosome preparations were silver stained (Howell and Black 1980) to verify the morphology of the chromosome 2 that carries the nucleolus organizer region in this species. Embryo karyotypes initially were scored independently from the females and then checked for discrepancies against the karyotype of the female. Ambiguous cases were then reexamined. Macrochromosomal karyotypes of all females are presented in the Appendix. Karyotypes of embryos are available from the authors. Specimens were cataloged and deposited as described by Sites et al. (1995) exceptfor additional material cataloged into the Museum of Zoology, Faculty of Sciences, Universidad Nacional Autonoma de Mexico (MZFC).
Clutch Size, Fecundity, and Fitness
Females with karyotypes assignable to the F5 cytotype were on average larger than females with either FM2 or intermediate karyotypes (table 1). Mean SVL for the two parental groups (57.58 and 50.56 mm for F5 and FM2, respectively) were significantly different (Mann-Whitney U, Z = 4.89, P [less than] 0.001). Snout-vent lengths of females with intermediate karyotypes spanned the range of the values for the two parental groups. However, the average SVL of these females (54.86 mm) was significantly lower than F5 females (57.58 mm, Z = 2.00, P = 0.0225), and significantly higher than FM2 females (50.56 mm, Z = 4.39, P [less than] 0.001). Although no significant relationship exists between female size and the number of heterozygous chromosomal markers (table 1), females heterozygous at two chromosomes (HM = 2) were on average larger (58.00 mm) than the F5 females (Z = 0.21 P = 0.4168).
Clutch sizes of the females examined in this study were similar to those reported for female Sceloporus grammicus from a separate locality (Ortega and Barbault 1984) where clutches averaged 6.17 embryos/female. The three female groups (F5, FM2, and intermediates) had very similar clutch sizes (table 1). Clutch sizes of FM2 females averaged larger than those of the F5 group (5.20 and 5.16, respectively); however, this difference was not significant (Z = 0.13, P = 0.4478). Likewise, the clutches of intermediates averaged slightly larger (5.33) than both the F5 and FM2 females. Again, the differences were not significant (Z = 0.34, P = 0.3671 and Z = 0.24, P = 0.4071 for intermediates versus F5 and FM2, respectively).
As demonstrated in several other sceloporines (Tinkle et al. 1970; Tinkle and Ballinger 1972; Ballinger 1973; Guillette and Sullivan 1985; Mendez de la Cruz et al. 1988), clutch size depends on female body size (SVL). Similarly, clutch size in the parental groups from the Tulancingo zone was highly correlated with SVL [ILLUSTRATION FOR FIGURE 2 OMITTED]. Simple linear regression analysis revealed that approximately 75% ([R.sup.2] = 0.7506) of the variation in clutch size of F5 females was explained by variation in body size [ILLUSTRATION FOR FIGURE 2A OMITTED]. Comparable regression parameters ([R.sup.2] = 0.7783) were reported for female S. grammicus from near the Michilia Biosphere Reserve, Durango, Mexico (Ortega and Barbault 1984). A substantial portion of the variation ([R2.sup.] = 0.6314) for FM2 females [ILLUSTRATION FOR FIGURE 2B OMITTED] also could be attributed to size, although the relationship was less robust. In intermediates only 26% ([R.sup.2] = 0.2558) of the variation was directly attributable to differences in body size [ILLUSTRATION FOR FIGURE 2C OMITTED].
Based on the regression analysis, F5 females gained an average of one embryo for each additional 2.94 mm of body length [ILLUSTRATION FOR FIGURE 2A OMITTED]. The gain for intermediates was one embryo for every 4.35 mm, whereas the ratio for FM2 females (1 embryo/3.45 mm) was higher than the intermediates but lower than that for the F5 group. This result is expected because the FM2 group likely contains some nonparentals (i.e., females [TABULAR DATA FOR TABLE 1 OMITTED] heterozygous at chromosome 3 and not 4). These values are consistent with those from other sceloporines in which the average clutch size increased by one embryo for each 23 mm increase in SVL (Marion and Sexton 1971; Ballinger 1973).
When grouped by the number of heterozygous marker chromosomes, three classes of intermediates (HM = 0, 1, and 2), comprising various non-[F.sub.1] females, produced clutches averaging larger than the parental groups (table 1). This result is expected in the HM = 2 class because of the larger body size. However, the values for the other classes (HM = 0 and 1) cannot be similarly explained. The HM = 3 class, comprising five [F.sub.1] females and one female recombinant at chromosome 2, included the four females (MZFC 4840(31), BYU 43101, BYU 43116, and IBH 7520-6) producing the smallest clutches among the intermediates (bottom four solid circles in [ILLUSTRATION FOR FIGURE 2C OMITTED]). This group produced the smallest average clutches despite an average body size comparable to the other groups.
The number of viable embryos per clutch was approximately equal for the two parental groups (table 1). The average number of viable embryos for the intermediates was only slightly lower than the parental groups, and pairwise comparisons with the parental groups showed that these differences were not significant (Z = 1.14, P = 0.1273 and Z = 1.48, P = 0.070 for intermediates versus F5 and FM2, respectively). However, in contrast to the parental groups in which the proportion of viable embryos was high (99.1% and 97.2% for F5 and FM2, respectively), only 80% of the embryos from the intermediates were viable.
As with total clutch size, the most precipitous drop in the number of viable embryos was seen in the most heterozygous females (HM = 3). In the HM = 3 females, the number of viable embryos per clutch averaged 1.33. This net decrease of 1.5 embryos per clutch becomes even more acute in light of the group's already reduced clutch size. The proportion of viable embryos in the HM = 3 females averaged just 0.417 (table 1). The combined effect of decreased clutch size and increased zygotic lethality is evident in figure 2D. The regression parameters of figure 2D were similar to those of figure 2C except for the depression in the regression line reflecting the average reduction in clutch size (table 1). Females in the HM = 3 group (mostly [F.sub.1] karyotypes near the center of the zone) and those of the HM = 2 group now make up the majority of the females falling below the regression line [ILLUSTRATION FOR FIGURE 2D OMITTED].
Although the average number of inviable embryos was very similar across all females, intermediates displayed a notable increase in the incidence of inviability. As shown in figure 3, the difference in viability becomes even more dramatic when the number of affected females is considered. Whereas in the F5 and FM2 groups the number of females in which all embryos were viable was near 90%, the same could be said for only 50% of the intermediates. As demonstrated by Sites et al. (1995), the incidence of inviability is greater for all females regardless of karyotype near the center of the zone.
The average number of viable embryos can be used to estimate the fitness of the various female groups. Using the viability of the F5 females as a benchmark, the effective fecundity (EF) of females from the FM2 and heterozygous marker (HM) groups was calculated by dividing the number of viable embryos for the group by the average for the F5 group (table 1). Comparison of EF values indicates that the FM2 and HM = 0-2 groups are approximately equal in fitness to the F5 females. In contrast, the HM = 3 group, which includes all F1 females, shows an almost 75% reduction in fecundity as compared to the F5 females.
Reproductive parameters of the intermediate group were further investigated to determine if a decrease in fecundity could be attributed to heterozygosity at particular marker chromosomes. The Multivariate General Linear Hypothesis (MGLH) option of SYSTAT was used to examine the effect of heterozygosity at individual marker chromosomes on reproductive parameters (table 2). Marker chromosomes were added to the regression model as categorical variables. An analysis of variance (ANOVA) on the clutches of intermediates showed no significant effects for individual chromosomes, [TABULAR DATA FOR TABLE 2 OMITTED] however, the two-way interaction (chrml x chrm6) and the three way interaction (chrml x chrm2 x chrm6) terms were significant. An ANOVA on the number of viable embryos showed significant effects for heterozygosity at chromosome 2 and for the same interaction terms in the analysis of total clutch (chrml x chrm6; and chrml x chrm2 x chrm6; table 2). With one exception (BYU 43121), females heterozygous at chromosomes 1 and 6 were also heterozygous at chromosome 2, and this may account for the significance of the chrml x chrm6 interaction term.
In these analyses, heterozygosity at chromosome 2 included both parental combinations (A[B.sub.d]) and recombinants ([AR.sub.c]). Comparison of the clutches of females heterozygous at chromosome 2 shows that the average number of embryos per clutch was lower for A[B.sub.d] females (4.14 embryos per clutch) than for [AR.sub.c] females (5.25 embryos per clutch). Likewise, the number of viable embryos was reduced by nearly 50% in the clutches of A[B.sub.d] females (2.43) as compared with [AR.sub.c] females (4.0). The proportion of inviable embryos was high (43.9%) for females heterozygous at chromosome 2; however, this proportion is likely influenced by the overall reduction in clutch size.
Complete macrochromoscomplements were scored from 242 of the 267 embryos karyotyped. Partial complements were scored for 14 of the remaining 25 viable embryos. Included in the total sample were four embryos with triploid karyotypes. These embryos were from two separate progenies (females MZFC 4840 and IBH 7522-8) both of which contained normal diploid embryos in addition to the triploids. We do not know the degree of aneupioidy in our sample. It is likely that some of the 25 embryos with unscorable karyotypes and some of the 34 inviable embryos taken from the same clutches were aneuploid.
TABLE 3. Comparison of chromosomal frequencies among progenies of female lizards heterozygous at chromosomes 1, 2, or 6. Included for each chromosome are the number of progenies examined, the total number of homozygous and heterozygous embryos, and the results of [[Chi].sup.2] analysis.
Chromosome 1(AB) 2([AR.sub.c]) 6(AB)
Progenies tested 21 4 14 Homozygotes 31 7 26 Heterozygotes 53 8 21 [[Chi].sup.2] 5.762 0.063 0.532 Probability 0.016 0.802 0.466
Chromosomal frequencies among the embryos were used to test for the loss of specific chromosomal morphologies. The number of homozygotes and heterozygotes in progenies from female lizards heterozygous at chromosomes 1, 2, or 6 were summed and the totals subjected to [[Chi].sup.2] analysis (table 3). The structural differences at chromosome 2 between the parentals necessitate a priori knowledge of the rate of recombination in calculating expected frequencies for A[B.sub.d] het-erozygotes. Because recombination cannot be estimated independent of the embryo karyotypes, comparisons were not performed on the clutches from these females. However, females with other heterozygous combinations at chromosome 2 and/or heterozygous at the other markers should produce an equal number of homozygous and heterozygous offspring regardless of the sire. Whereas this was the case for one combination at chromosome 2 ([AR.sub.c]) and for chromosome 6, the analysis found a significant excess of embryos heterozygous at chromosome 1. This excess of heterozygous embryos is exemplified in the clutches of two females (IBH 7518-7 and BYU 43088); both of these females were heterozygous at chromosome 1 but produced greater than expected numbers of heterozygous embryos (5 of 5 and 4 of 5, respectively).
Previous investigations (Mrongovius 1979; Barton 1980; Shaw and Wilkinson 1980; Searle 1984; Hewitt et al. 1987; Redi and Capanna 1988; Garagna et al. 1990) have provided fundamental information regarding the effects of chromosomal heterozygosity on the fecundity of hybrid females. Although little is still known of the degree of actual infertility of vertebrates in nature, studies of the meiotic behavior of Robertsonian rearrangements have provided insight into the potential role of these rearrangements as reproductive isolating mechanisms. In most cases, the actual consequences of any observable meiotic disruption on fecundity could only be inferred.
A few studies have attempted to measure the effect of Robertsonian heterozygosity on fertility by assessing the condition of embryos. However, most of these investigations focused on the fertility of male carriers when crossed to normal females (Long 1977; King et al. 1981). Wallace et al. (1991) examined oogenesis in the common shrew (Sorex araneus) and found only small differences between homozygotes and Robertsonian heterozygotes. Searle (1990) provided one of the first detailed examinations of pregnant females of the same species (S. araneus) taken from within a Robertsonian hybrid zone. Searle compared the number of ovulations, regressing implants, and fetuses from females homozygous and heterozygous for both "simple" and "complex" Robertsonian rearrangements. This work concluded that the overall fertility of females from within the hybrid zone was not substantially different from females outside the zone.
Dual effects on fertility often accompany hybridization (Gropp et el. 1982; Searle 1993). Hybrids may display increased levels of primary infertility (germ cell death), or secondary infertility (early death of progeny) evident as inviable embryos. Whereas primary infertility is likely the result of aberrant chromosome pairing in pachynema, secondary infertility is caused by genetic imbalance resulting from realsegregation (aneuploidy). In addition, other secondary factors such as maternal effects or genetic incompatibility may cause embryo lethality. The present study demonstrated that Sceloporus grammicus females with [F.sub.1] chromosomal phenotypes are fertile. However, these females were substantially less so, producing smaller clutches with higher levels of embryo mortality. Thus, both primary and secondary factors seem to be operating within the Tulancingo hybrid zone.
Analysis of reproductive data from females supports the hypothesis that heterozygosity at chromosome 2 is an important determinant of fecundity. Reed et al. (1995b) found altered recombination and increased aneuploidy in males heterozygous for the parental morphologies at this chromosome (A[B.sub.d]). As in the females, significant effects were not thought to be attributable to heterozygosity at chromosomes 1 and 6. The production of an average sized clutch by one [F.sub.1] female (BYU 43104, Appendix), however, suggests that the reduction in clutch size cannot be entirely attributed to chromosomally based infertility. The general increase in the incidence of embryo inviability for all females (intermediates and parentels) near the center of the hybrid zone (Sites et al. 1995) indicates that secondary infertility is also occurring.
Comparison of clutch sizes indicates that the genetic background of the sire may be an important factor in determining female reproductive success. For example, differences in the size of clutches of the most heterozygous females (HM = 3) suggests that offspring can be "rescued" by introducing an intact gene system that can compensate for the dysfunctional recombinant genome inherited from the mother. Rescue is achieved if the female backcrosses to a more "parental" type. For example, the HM = 2 (BYU 43109, IBH 7520, IBH 7520-5, and BYU 43121) and HM = 3 (BYU 43104) heterozygotes producing the most viable progeny appeared to have mated with males with less heterozygous karyotypes based on the karyotypes of their embryos.
Hybrid breakdown may be caused by disruption of epistatic interactions between coadapted nuclear genes (Dobzhansky 1970; Wallace 1991). This would have little affect on [F.sub.1] hybrids but would become apparent in the [F.sub.2] or later generations. The effect of such processes were eloquently demonstrated in the hybrid zone involving taxa of Caledia captive (Shaw et el. 1990). The Moreton and Torresian taxa differ by fixed pericentric inversions at 7 of 12 chromosomal pairs. Analysis of crosses between the taxa showed that fertility and viability of the [F.sub.1] generation did not differ from the parentals (Shaw and Wilkinson 1980). The [F.sub.2] generation was completely inviable, but viable progeny could be produced if [F.sub.1] females were backcrossed to parentels. Reciprocal crosses involving [F.sub.1] males again resulted in no viable progeny. This mortality of [F.sub.2]s was not attributed to meiotic disruption caused by chromosomal heterozygosity but rather to the generation of imbalanced recombinant chromosomes during meiosis in the [F.sub.1] parent. The reproductive dynamics of the Tulancingo hybrid zone share several aspects of the Caledia zone.
Fecundity differences among the females examined in the present study are suggestive of different coadapted gene complexes in the F5 and FM2 cytotypes. Molecular studies show some divergence between the genomes of these cytotypes in nuclear markers (allozyme frequency differences at several loci, a fixed restriction site difference in ribosomal DNA repeats for the enzyme Xmn I, and a possible gene duplication at the G3PDH locus in the F5 race), and considerable divergence in the mitochondrial DNA genomes (Sites et al. 1993). Given these levels of overall genetic divergence between these cytotypes, different coadapted gene complexes may have accumulated. Hybrid breakdown, evident as decreased embryo viability, may be the result of the disruption of these complexes during oogenesis in [F.sub.1] females or during embryonic development. As a result, [F.sub.1] females are substantially less fertile than both parentals and other chromosomal intermediates. The study by Sites et el. (1995) suggests that mating is random within local neighborhoods, dispersal is limited, but the clines for all three marker chromosomes are narrow relative to dispersal capabilities of S. grammicus. Sites et al. (1995) concluded that both genetic drift and habitat selection contributed to zone structure. In the absence of assortative mating, the steep concordance in clines is likely maintained by selection against the hybrids. Part of this selection is probably due to effects associated with chromosome-2 heterozygosity, but results of this study also clearly implicate genic effects in the reduction of fitness in hybrid females.
We thank E. Arevalo, I. Goyenechea, F. Mendoza, D. Mink, and M. Mancilla for assistance with specimen collection and processing. E. Adams, J. Bickham, and J. Werren provided use of microscope and/or computer facilities, and B. McAllister critically reviewed the manuscript. This research was supported by a grant from the United States National Science Foundation (BSR-8822751).
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[TABULAR DATA FOR APPENDIX OMITTED]
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|Author:||Reed, Kent M.; Sites, Jack W., Jr.|
|Date:||Feb 1, 1995|
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