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2 Department of Biological Sciences, Texas Tech University, Lubbock, Texas 79409 USA; and 3 Department of Biology, Vanderbilt University, Nashville, Tennessee 37235 USA
Received for publication January 19, 1999. Accepted for publication October 14, 1999.
ABSTRACT
As has been shown for many kinds of organisms, barriers to interspecific hybridization may differ in strength between reciprocal crosses, resulting in a bias in the probability that one or the other species may be the maternal or paternal parent of hybrids. The fern Dryopteris Xtriploidea, the "backcross" hybrid between the diploid D. intermedia and the tetraploid D. carthusiana, occurs in large numbers in nature, providing an opportunity to investigate whether such a bias exists. Differences in the chloroplast genome distinguishing the two parental species were discovered in the sequence of the trnL region following amplification by polymerase chain reaction (PCR), including a Mse I restriction site. This allowed rapid identification of the donor of the chloroplast genome, and therefore the maternal parent of each hybrid, assuming chloroplast DNA to be maternally inherited in Dryopteris. Analysis was carried out on 127 hybrids, shown to be of independent origin using allozymes, occurring at three localities in Virginia and West Virginia. When samples from all localities were pooled, 91 possessed the D. carthusiana trnL genotype and 36 possessed the D. intermedia genotype, a ratio that is significantly different (P < 0.001) from the null hypothesis of no gender bias. The strength of the bias differed significantly among the three sites, however, with bias at the West Virginia site much stronger (5.6:1 carthusiana:intermedia; P < 0.001) than at either Virginia site (1.55:1 and 1.43:1 carthusiana:intermedia, respectively; P > 0.05 in both cases). The cause of the strong bias in the West Virginia sample is unknown, as is the cause of the population differences. Causes of bias could include differences between the parental species related to their ploidy difference, including sizes of gametes and/or gametangia, sperm motility, breeding system (D. intermedia is outcrossing while D. carthusiana is selfing), or the nature and strength of interspecific isolating mechanisms.
Key Words: chloroplast DNA • Dryopteris • fern hybrid • isolation mechanism • polyploid • trnL sequence • unilateral hybridization
Interspecific mating results from the failure of reproductive isolating mechanisms that ordinarily would prevent hybridization. Because the strength of such mechanisms could differ in reciprocal crosses, it is conceivable that the likelihood for hybridization between a given pair of species would be different for reciprocal matings, and indeed such a gender bias in hybridization events has been demonstrated for various kinds of organisms (Kaneshiro, 1990
; Bradley, Davis, and Baker, 1991
; Lehman et al., 1991
; Page, Chapman, and Jennetten, 1991
; Bella et al., 1992
; Harder, Cruzan, and Thomson, 1993
; McConchie, Vithanage, and Batten, 1994
; Emms, Hodges, and Arnold, 1996
; Hannan and Prucher, 1996
; Sedgley, Wirthensohn, and Delaporte, 1996
; Weiblen and Brehm, 1996
; Jansson and Ost, 1997
; Avise et al., 1997
; Carracedo et al., 1998
; Vogel et al., 1998a
).
Despite the widespread occurrence of hybridization in ferns (Knobloch, 1976
), neither the reproductive isolating mechanisms that limit mating between fern species, nor the extent of gender bias that might exist when ferns do hybridize, are well studied. The simple microscopic mating apparatus and process whereby flagellated sperms swim through water into the necks of archegonia provide few clues as to what might cause matings to fail, although evidence for chemical incompatibility interactions has been implicated for wide crosses (Schneller, 1981
). In one of the few large-scale studies of gender bias during fern hybridization, Vogel et al. (1998a)
used maternally inherited chloroplast DNA (cpDNA) fragments to show that Asplenium septentrionale was the maternal parent in >95% of the hybrid A. xalternifolium individuals examined. It is not yet clear whether such strong gender bias is a common feature of fern hybridization. In this paper we also use patterns of cpDNA variation to investigate the potential for gender bias in the interspecific matings leading to the formation of hybrids in the fern genus Dryopteris. Patterns of chloroplast transmission were studied at three localities, providing the opportunity for us to detect any population specificity in degree of bias.
Dryopteris is one of the most hybrid-prone plant genera in temperate regions, as evidenced by 25 different interspecific combinations of sterile hybrids known from eastern North America (Wagner, 1971
; Montgomery and Wagner, 1993
), as well as an intergeneric hybrid between a Dryopteris species and a species in the sister genus Polystichum (Wagner et al., 1992
). Although most of these are of rare occurrence, certain hybrid combinations are surprisingly common, especially that between two wide-ranging common species, D. intermedia (Muhl.) A. Gray and D. carthusiana (Villars) H. P. Fuchs. These two parental species are related as diploid ancestor D. intermedia (genome formula II) and allotetraploid derivative D. carthusiana [genome formula IISS; the S genome is derived from the extinct species D. "semicristata" (Wagner, 1971
; Hutton, 1992
; Werth and Lellinger, 1992
; Werth, unpublished data)]. Thus, the hybrid is a "backcross" triploid with the genome formula IIS, and is often referred to by the validly published binomial D. xtriploidea Wherry.
One of the commonest hybrids of any kind in eastern North America, Dryopteris xtriploidea usually can be found at the numerous localities where both parental species co-occur, and occasionally even where only one parent occurs, through much of the Appalachian provinces, the Great Lakes area, and southern Canada. The hybrids often occur in strikingly large numbers, sometimes outnumbering the parental species and creating confusion as to species boundaries (Tryon and Britton, 1966
). Although hypothesized to be capable of reproduction through apogamy (De Benedictis, 1969
), isozyme markers indicate that each D. xtriploidea plant in such arrays is a first-generation hybrid of independent origin (Werth and Xiang, unpublished data). This abundance of hybridization events provided an opportunity to evaluate the gender directionality of numerous matings between these two species, provided that maternally inherited markers could be obtained.
The feasibility of the present study was bolstered by evidence that cpDNA is maternally inherited in ferns (Stein and Barrington, 1990
; Gastony and Yatskievich, 1992
; Vogel et al., 1998b
), and that the chloroplast genomes of D. intermedia and D. carthusiana are genetically distinct (Hutton, 1992
). Although allopolyploids may acquire the chloroplast genomes of both of their progenitors through multiple origins (Soltis and Soltis, 1989
), the chloroplast genome of D. carthusiana is apparently derived only from that of its diploid ancestor, D. "semicristata," a feature it shares with another allotetraploid D. cristata, which is derived from hybridization between D. ludoviciana and D. "semicristata" (Hutton, 1992
). Isozyme evidence suggests that D. carthusiana had a unique origin (Werth and Haufler, unpublished data), which may have precluded its ever obtaining the chloroplast genome of D. intermedia, its other ancestor. To obtain markers for our study, we turned to the group I intron within the chloroplast DNA gene trnL(UAA) (Taberlet et al., 1991
), which has been found often to exhibit differences between closely related species (Böhle et al., 1994
; Gielly and Taberlet, 1994a, b
), as well as being variable within species (McCauley et al., 1996
). Thus, examination of the cpDNA haplotype found in numerous D. xtriploidea individuals allowed us to ask whether a species bias exists in the transmission of the chloroplast genome during hybridization between D. intermedia and D. carthusiana, and whether the relative contribution of the two species to hybrid populations varies among localities. With the assumption of maternal inheritance of cpDNA, we can further ask whether there is evidence of gender bias during hybridization.
MATERIALS AND METHODS
Collection
Leaf samples of both parental species, D. intermedia and D. carthusiana, were collected from several different localities in Virginia and West Virginia (Table 1). Hybrid D. xtriploidea plants also were collected at three of these localities—Hanging Rock, West Virginia, and Falls Church and Interior, Virginia—where they were found to be exceptionally numerous (Table 1). Voucher specimens are on deposit in the E. L. Reed Herbarium at Texas Tech University (TTC). Discrimination between the two parental species and their hybrid in the field is possible but achieved with some uncertainty due to their similarity in leaf form. However, all collections were diagnosed unequivocally based on microfeatures examined in the laboratory (glandular trichomes abundant in D. intermedia, absent in D. carthusiana, and frequent in the hybrid; spores larger in D. carthusiana than D. intermedia, aborted in the hybrid). Isozyme genotypes of the hybrids were also obtained to verify both their correct identification and their independent formation (Xiang and Werth, 1996
; Werth and Xiang, unpublished data).
|
) as modified by McCauley et al. (1996)
. Polymerase chain reaction (PCR) using the "c" and "d" PCR primers described by Taberlet et al. (1991)
was used to amplify an ~600-bp (base pair) region of the trnL (UAA) chloroplast gene that includes a group I intron. PCR products from representative individuals of both parental species and hybrids were sequenced on an ABI 377 automated sequencer (Perkin Elmer Corp., Foster City, California, USA) using the ABI dye terminator kit according to the manufacturer's protocol. Both strands were sequenced using "c" and "d" as sequencing primers. Sequences were then compared following manual alignment. Based on species-specific sequence differences revealed by this comparison, discrimination between trnL genotypes was then routinely accomplished by digestion of PCR products with the restriction enzyme Mse I (which recognizes the DNA sequence TTAA), and electrophoresis of the resultant fragments on 4% Metaphor agarose gels stained with ethidium bromide. Following Vogel et al. (1998b)
, PCR was also carried out using deliberately mixed templates of both D. intermedia and D. carthusiana to evaluate whether a heteroplasmic cpDNA genotype (such as might result from biparental inheritance) could be detected by the PCR method.
Statistical analysis
Our statistical null hypothesis was that any observed deviation from a 1:1 ratio of carthusiana:intermedia in the cpDNA haplotypes found in hybrids was due to sampling error and not a real bias. To test this we employed the Replicated G Goodness-of-Fit statistic (Sokal and Rohlf, 1995
, p. 715). This allows deviations from 1:1 to be investigated for all observations pooled across populations, as well as on a population-by-population basis. Importantly, it also allows us to ask whether the ratio varies from population to population (Ghet test for heterogeneity; Sokal and Rohlf, 1995
). In the event that there is among-population heterogeneity, the Ghet statistic can be used further to compare subsets of populations.
RESULTS
Discriminaton of parental species
The amplified trnL regions of D. intermedia and D. carthusiana were very similar in size and sequence, differing by two length (insertion/deletion) mutations and occasional substitutions that included a difference in the number of Mse I restriction sites; there is one Mse I site in D. intermedia and two in D. carthusiana (Fig. 1). Digestion using Mse I therefore resulted, as would be predicted, in two fragments of lengths ~400 kb (kilobase) and 260 kb in D. intermedia, vs. three fragments of lengths 310, 260, and 90 kb in D. carthusiana (Fig. 2). Identical within-species restriction patterns were obtained for all 45 D. intermedia and all 44 D. carthusiana individuals examined, and thus were inferred to represent highly consistent phenotypes that reliably discriminate between the two parental species. These results are consistent with a RFLP (restriction fragment length) study that found consistent restriction site differences distinguishing D. intermedia and D. carthusiana chloroplast genomes (Hutton, 1992
). PCR phenotypes resulting from reactions with deliberately mixed templates exhibited all four expected bands, indicating amplification of trnL from both genomes.
|
|
; Vogel et al., 1998b
). Of the 127 hybrids examined at both sites, the majority (91) possessed the D. carthusiana trnL genotype, while a minority (36) possessed the D. intermedia genotype, resulting in a stongly biased ratio of 2.53:1 that was highly statistically different from the 1:1 expectation for no gender bias (null hypothesis) (Table 1). While the majority cpDNA genotype in hybrids at all sites was that of D. carthusiana, the ratios differed among the three sites. At the Hanging Rock, West Virginia site the ratio of carthusiana to intermedia cpDNA genotypes (5.6:1) was much higher than that at Falls Church or Interior, Virginia, where the respective ratios (1.43:1 and 1.55: 1 carthusiana:intermedia) were not statistically distinguishable from 1:1 (Table 1). The difference in ratio among the three sites was found to be highly significant (Ghet = 9.69, df = 2, P < 0.01). Given significant heterogeneity among the three population ratios, the two Virginia sites were next compared to each other and found to be statistically similar in ratio (Ghet = 0.02, df = 1, P > 0.50). Data from the two Virginia sites were then pooled and compared to the West Virginia site. This last comparison was statistically significant (Ghet = 9.67, df = 1, P < 0.01). Thus, the relative rate of transmission of cpDNA from the respective parental species to the hybrid is different at the West Virginia site compared to the Virginia sites, and the deviation from the 1:1 null expectation found in the overall pooled data set is due almost entirely to the influence of the West Virginia sample. DISCUSSION
The results demonstrate that, pooled across localities, the chloroplast genome found in D. xtriploidea is inherited from D. carthusiana more often than from D. intermedia. However, the degree of bias in inheritance is clearly population dependent. While the carthusiana haplotype was in the clear majority in hybrids collected from West Virginia, neither Virginia site differed statistically from 1:1 in its own right or from each other (though carthusiana-derived haplotypes still predominated in each case). This is in contrast to a recent study of the fern hybrid Asplenium xalternifolium in which Vogel et al. (1998a)
observed a nearly complete bias (28:1), with the maternal ancestor of most hybrids being the tetraploid Asplenium septentrionale subsp. septentrionale rather than the diploid A. trichomanes subsp. trichomanes. Their observation was consistent across populations. No bias was detected in a study of chloroplast DNA in hybrids between diploid Polystichum acrostichoides x tetraploid P. braunii (Stein and Barrington, 1990
), however, the sample size of four individuals (two each for either parental chloroplast genotype) was too small for statistical analysis. Our observations of D. xalternifolium raise the following questions: (1) does the bias in chloroplast transmission (when it exists) reflect a bias in the maternal ancestry of D. xtriploidea? (2) what mechanisms might generate such a bias? and (3) why do those mechanisms operate strongly in some populations and not others?
In using the trnL region from the chloroplast genome as a marker for maternal ancestry, we have assumed that cpDNA is maternally inherited in the Dryopteris hybrids we examined, as it is in the vast majority of plants (Birky, 1995
). This assumption was in part validated by our finding of only one or the other species-diagnostic trnL chloroplast genotype in each D. xtriploidea hybrid, whereas both genotypes appeared in PCR reactions when deliberately mixed templates were used. Evidence of uniparental inheritance of chloroplast genomes in ferns derives from microscopic studies of organellar transmission in Pteridium (Duckett and Bell, 1971, 1972
) and Pteris (Kuroiwa, Sugai, and Kuroiwa, 1988
), and from cpDNA studies of interspecific hybrids in Osmunda (Stein, 1985
), Polystichum (Stein and Barrington, 1990
), the latter genus very closely related to Dryopteris (Wagner et al., 1992
), as well as a series of hybrids between apogamous (male) and sexual (female) species of cheilanthoid ferns (Gastony and Yatskievich, 1992
). More recently, Vogel et al. (1998b)
experimentally demonstrated maternal inheritance of cpDNA in Asplenium and provided an explanation to dismiss the earlier suggestion of biparental inheritance in this genus (Andersson-Kötto, 1930
). Our results suggest that the inheritance of cpDNA in Dryopteris is uniparental. Given evidence for maternal inheritance in several other species of ferns, we proceed with the assumption of maternal inheritance of cpDNA in Dryopteris.
What mechanisms might generate gender bias? In angiosperms, there is a consistent relationship between the directionality of bias and differences between the breeding systems of species participating in hybridization: self-incompatible species are able to function as pollen parents of hybrid seeds in the flowers of self-compatible species, but not the reverse, a condition referred to as unilateral interspecific incompatibility or the "SI x SC rule" (Harrison and Darby, 1955
; Lewis and Crowe, 1958
; de Nettancourt, 1977, 1984
; Harder, Cruzan, and Thomson, 1993
; reviewed by Arnold, 1997
). The causal basis for the bias in the present study is far from obvious, and in fact may be the net effect of a number of contrasting factors. The two Dryopteris species differ not only in ploidy but also in their breeding system and associated sex expression in gametophytes. As in the majority of diploid fern species (Soltis, Soltis, and Holsinger, 1988
), D. intermedia possesses an outcrossing mating system, as evidenced by concordance of populational genotype frequencies to Hardy-Weinberg expectations (Werth, unpublished data). Moreover, D. intermedia gametophytes tend to be unisexual, with sex expression mediated by the pheromone antheridiogen (Werth and Cheav, unpublished data). In contrast, D. carthusiana appears to be predominantly selfing as evidenced by severe heterozygote deficiencies at polymorphic loci (Werth and Haufler, unpublished data), a feature it shares with many other polyploid ferns (Masayuma and Watano, 1990
). Gametophytes of D. carthusiana tend to be hermaphroditic (Werth and Yun, unpublished data), but it is presently unknown whether they respond to antheridiogen.
We initially predicted that a bias might result from the difference in breeding systems of the two Dryopteris species, but in the opposite direction from that encountered in angiosperms as discussed above. We hypothesized that because eggs of the outcrossing species Dryopteris intermedia are usually fertilized by foreign (non-self) sperm, while those of the inbreeding D. carthusiana are usually fertilized by self sperm, the outcrossing species would have a higher probability to be a mother in interspecific mating events (Xiang et al., 1997
). Vogel et al. (1998a)
posed essentially this same hypothesis, emphasizing synchronous gamete release, to explain the strong bias for maternal ancestry by outcrossing Asplenium septentrionale, rather than inbreeding A. trichomanes, in hybridizations resulting in A. xalternifolium. However, this hypothesis clearly fails to explain the observed gender bias for the present study, in which the self-fertilizing species D. carthusiana was more often the maternal parent, at least in the West Virginia population. An alternative hypothesis is that selfing over many generations may have selected for reduced sperm motility in D. carthusiana, reducing its potential to serve as a father in hybrid crosses. Moreover, antheridiogen-mediated sexual dimorphism in D. intermedia could mean that only a subset of gametophytes can serve as mothers, in contrast to the opportunity of female function for most or all of the hermaphroditic D. carthusiana gametophytes.
It is possible that the differences in ploidy per se could have contributed to the observed bias, as larger cell sizes associated with polyploidy might influence the physical attributes of gametangia and/or motility of sperms. Sperms of the tetraploid D. carthusiana might be larger and perhaps slower, and might not as easily enter the presumably smaller archegonial opening of the diploid D. intermedia. On the other hand, D. carthusiana sperms might benefit in vigor from being diploid and possessing a high degree of heterozygosity in contrast to the haploid sperms of D. intermedia. Additional factors that could influence gender bias include timing of gametangial maturation, differential survivorship of hybrids formed through reciprocal crosses (e.g., hybrid zygotes that possess D. carthusiana cytoplasm may be more likely to mature), and ecological setting. Differences in spatial arrangement and/or population density between the two parental species could influence the reciprocal sperm to egg ratios within gametophyte cohorts. Soil type might also have some influence.
Of course it is entirely possible that the observed gender bias in hybridization was influenced by virtually all the above factors, some of them genetically determined, others environmental, with factors favoring opposite biases resulting in a net effect that varies among sites. A more precise understanding will only emerge from more detailed studies of the still poorly understood mating process in ferns and the reasons for reduced success rates of interspecific crosses, i.e., isolating mechanisms. The one population in which the observation of bias is so clearly supported shows that despite the formation of numerous hybrids, some form of isolating mechanism(s) indeed must exist, i.e., the two species do not interbreed indiscriminately.
Further investigation of gender-biased hybridization is merited, as it has a number of implications for evolutionary processes involving hybridization (Arnold, 1997
; Vogel et al., 1998a
). Chloroplast DNA has seen increased use in inferring origins of allopolyploid species from sterile interspecific hybrids and their subsequent evolutionary histories, often complementing data from morphology and isozymes (e.g., Soltis and Soltis, 1989
). A striking revelation of such studies is the general tendency for polyploid origin and evolution to have involved multiple hybridizations (Werth et al., 1985
; reviewed by Soltis and Soltis, 1993
). Multiple origins would be expected to result in incorporation of both parental chloroplast genomes into the allopolyploid gene pool, however, a consistent gender bias in hybridization such as demonstrated by Vogel et al. (1998a)
could result in only a single ancestral cpDNA genome being incorporated. Variation among populations for gender bias, as implicated in the present study, might lead to haphazard incorporation of both parental cpDNAs, equivalent to the result for a species pair lacking any tendency for such bias. On the other hand, if the variation for bias is geographically patterned, this pattern could be imposed on the distribution of cytoplasmic genotypes in the allopolyploid, leading to insights into the biogeographic history of the polyploid species. In any event, our results demonstrate the importance of considering multiple populations in any study of gender-biased hybridization.
FOOTNOTES
1 The authors thank Jennifer Stevens for developing the PCR and restriction digest protocols, Holiday Wagner for help in locating the Interior, Virginia site, Jim Leebens-Mack for assistance with sequencing, Cynthia Caplen for assistance in collection and diagnosis of hybrids, and Robert Bradley for helpful discussions. This research was supported by National Science Foundation Grants DEB 9220755 awarded to CRW and DBI 9604814 awarded to DEM. A significant portion of this work was carried out at the Mountain Lake Biological Station, Pembroke, Virginia, and we are grateful for the substantial logistical support provided by the station. 
4 Author for correspondence (e-mail: mccaulde{at}ctrvax.vanderbilt.edu
).
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