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Annals of Botany 92: 647-655, 2003
© 2003 Annals of Botany Company

Allozymic Differentiation of the Antirrhinum graniticum and the Antirrhinum meonanthum Species Groups

I. MATEU-ANDRÉS*,1 and J. G. SEGARRA-MORAGUES2

1 Instituto Cavanilles de Biodiversidad y Biología Evolutiva, C/Dr. Moliner 50-E46100-Burjassot, Valencia, Spain and 2 Departamento de Agricultura y Economía Agraria, Facultad de Veterinaria, Universidad de Zaragoza, C/Miguel Servet 177, E50013-Zaragoza, Spain

* For correspondence. E-mail Isabel.mateu@uv.es

Received: 25 July 2002;; Returned for revision: 20 May 2003. Accepted: 24 July 2003; Published electronically: 10 September 2003


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 TAXONOMIC SYNTHESIS FOR THE...
 LITERATURE CITED
 

Forty populations from eight taxa belonging to six species of Antirrhinum were studied for electrophoretic differentiation at 14 allozyme loci. All the studied species show that marker alleles and genetic distances between conspecific populations are lower than for other species of the genus. Results permit the recognition of A. onubensis and A. boissieri at specific rank. The low level of genetic distance together with morphological characters and sympatric range, support the recognition of A. ambiguum as a new subspecies of A. graniticum, as A. graniticum ssp. ambiguum Mateu & Segarra stat. nov. The results of the study support separation of the studied taxa into two groups coinciding with subsections Streptosepalum and Antirrhinum, but disagreeing with the arrangement of species into them. According to the results of the study these groups consist of A. meonanthum and A. braun-blanquetii (Streptosepalum) and A. graniticum s.l., A. onubensis and A. boissieri (Antirrhinum). The status of A. meonanthum var. rothmaleri requires further clarification.

Key words: Snapdragons, Antirrhinum, allozymes, systematics.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 TAXONOMIC SYNTHESIS FOR THE...
 LITERATURE CITED
 
The old world genus Antirrhinum L. includes some 25 species, mainly distributed in the Iberian Peninsula (Sutton, 1988). The chromosome number has been studied in most of the species (Bolkhovskikh et al., 1969; Moore, 1982), A. graniticum and A. meonanthum included (Boscaiu et al., 2000; Gallego-Martín and Sánchez-Anta, 1986), being 2n = 16 in all species studied.

Rothmaler (1956) divided the genus into three subsections with several series. Recently, Fernández Casas (1997) restructured the genus, the main change being the elevation of subsections to sections and series to subsections, but his treatment was explicitly based on Rothmaler’s classification Rothmaler (1956). In this work Rothmaler’s system is followed.

The morphological discrimination of Antirrhinum species is complex in many cases (Sutton, 1988), leading to different views both in the discrimination of taxa and in the assignment of rank. Two of the more complex groups of species are those related to A. graniticum Rothm. and A. meonanthum Hoffgg. & Link (Table 1).


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  		Table 1. Comparison of the different taxonomic treatments of the studied taxa
 
Antirrhinum graniticum is included in subsection Antirrhinum (= section Antirrhinum following Fernández Casas). In one of the most recent treatments, Sutton (1988) considered the species to be divided into two subspecies: A. graniticum ssp. graniticum and A. graniticum ssp. brachycalyx Sutton. The type subspecies is distributed on various soil types and has a wide range, in the central area of the Iberian Peninsula. In contrast, A. graniticum ssp. brachycalyx prefers gypsum soils and has a narrow range, with only a few known populations close to Valdemoro (Madrid, Central Spain). Antirrhinum boissieri Rothm. (Rothmaler, 1956) is related to A. graniticum and its taxonomic position has been discussed. Webb (1971, 1972) considered it to be conspecific with A. graniticum, Valdés (1986) treated it as a subspecies of A. graniticum, and Sutton (1988) included it in A. hispanicum Chav. Fernández Casas (1997) recognized it at specific rank.

Subsection Streptosepalum Rothm. includes A. meonanthum Rothm., A. braun-blanquetii Rothm. and A. ambiguum Lange. Antirrhinum meonanthum includes two varieties, var. meonanthum and var. rothmaleri Pinto da Silva (Pinto da Silva, 1970). The latter is distinguished from the type variety by its larger corollas and capsules. This taxon has not been considered further in other taxonomic treatments of the group (e.g. Webb 1971, 1972; Sutton, 1988; Fernández Casas, 1997). Flower and inflorescence size, as well as the number of flowers per inflorescence, constitute clear differences between A. meonanthum and A. braun-blanquetii. However, differences in indumentum and bract size between A. meonanthum and A. ambiguum have been considered, and these led both Webb (1971) and Sutton (1988) to consider A. ambiguum as conspecific with A. meonanthum. Webb (1971) hypothesized that introgression from A. graniticum is responsible for some of the variation. Sutton (1988) commented that A. meonanthum has been frequently confused with the pink-flowered A. graniticum.

Antirrhinum onubensis Fern. Casas is restricted to a small area in the south-west of the Iberian Peninsula. It was first described as A. meonanthum ssp. onubensis Fdez. Casas (1982), but Fernández Casas (1987) later raised it to specific rank; and Valdés (1986) recombined it as A. graniticum ssp. onubensis (Fdez. Casas) Valdés. Fernández Casas (1987) considered it closer to A. graniticum.

Data from sequences of several genes support the hypo thesis that all the species of Antirrhinum are closely related (Vieira et al., 1999; Vieira and Charlesworth, 2001), sup porting the opinion that the low level of differentiation between Antirrhinum species is based on the accumulation of differences encoded by single genes combined with geo graphic barriers (several authors in Fernández Casas, 1997).

Allozymes are molecular markers that may be useful in establishing relationships at low systematic levels (Gottlieb, 1984; Crawford, 1985). Allozymes have been used to study several American genera of tribe Antirrhineae Dumort (Elisens and Crawford, 1988; Elisens, 1992; Elisens and Nelson, 1993) and in Antirrhinum they have proved to be useful molecular markers for species discrimina tion (Mateu-Andrés, 1999; Mateu-Andrés and Segarra-Moragues, 2000).

In this work, taxa related to A. graniticum and A. meonanthum are studied to establish their taxonomic delimitation and relationships. The previous use of different criteria for taxon delimitation and assignment into subsections and the potential introgression between A. graniticum and A. meonanthum (Webb, 1971) make it necessary to study all taxa together.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 TAXONOMIC SYNTHESIS FOR THE...
 LITERATURE CITED
 
Plant material
Seeds were sampled from 40 populations (Table 2; Fig. 1). Generally, seeds were sampled from between 25 and 50 % of the total number of mature plants in each population. Up to 30 seedlings per population were raised under glasshouse conditions. In all, 874 individuals were studied.


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  		Table 2. Sampled taxa and populations
 


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  		Fig. 1. Maps of distribution of the studied populations.

 
Electrophoresis and analysis
Electrophoresis was carried out on horizontal 10 % starch gels. The extraction buffer consisted of 0·2 M Tris–HCl pH 7·5, 2 mM EDTA, 0·12 M Na2S2O5, 1 M Cl2Mg, 40 mg ml–1 (w/v) PVP, and 4 µl ml–1 mercaptoethanol. Material used consisted of young leaves of plants grown in the glasshouse. Extracts were absorbed onto 3 mm wicks of Whatman chromatography paper.

Thirteen enzyme systems were assayed: aconitase (ACO), aspartate aminotransferase (AAT), diaphorase (DIA), esterase (EST), isocitrate dehydrogenase (IDH), malate dehydrogenase (MDH), malic enzyme (ME), menadione reductase (MNR), phosphogluconate dehydrogenase (6PGD), phosphoglucoisomerase (PGI), phosphoglucomutase (PGM), shikimate dehydrogenase (SKD) and triose-phosphate isomerase (TPI), and all except EST, ME and SKD gave banding patterns. 6PGD could not be scored due to its inconsistent banding patterns, and MDH could not be scored due to its complex banding pattern. The electrophoretic buffer system II of Wendel and Weeden (1989) was employed to resolve IDH, MDH, 6PGD and SKD; system VI for DIA, PGI, PGM and TPI; and system VII for AAT, ACO, MNR and 6PGD. All staining methods followed Wendel and Weeden (1989), except for AAT, which followed a modification by H. C. Prentice (pers. comm.).

Diversity parameters and genetic distance coefficients were calculated using BIOSYS-1 (Swofford and Selander, 1989). Routines in BIOSYS-1 were used to generate both UPGMA phenograms from Nei’s (Nei, 1972) and modified Roger’s (Wright, 1978) distances.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 TAXONOMIC SYNTHESIS FOR THE...
 LITERATURE CITED
 
Eight out of the 13 enzyme systems studied were interpreted, giving a total of 14 loci. The 14 scored loci gave a total number of 51 alleles which are summarized in Table 3 (original data are available upon request from Isabel.Mateu{at}uv.es). The most frequent alleles were in general shared by all the taxa studied. Five of them (DIA2-2, DIA4-2, MNR1-1, MNR2-1, TPI2-2) were fixed in the vast majority of populations (means across populations: 85, 92·5, 92·5 and 82·5 %, respectively). AAT1-2 was fixed in 45 % of the populations.


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  		Table 3. Summary of means and ranges of allele frequencies in the studied taxa
 
Two alleles were restricted to only one taxon each (i.e. ‘specific’), DIA1-2 to A. boissieri and DIA2-1 to A. meonanthum var. rothmaleri. DIA2-1 was fixed in that taxon, in contrast to all other taxa in which allele DIA2-2 is fixed. It is noteworthy that DIA1-1 was fixed in A. meonanthum var. rothmaleri, but was also present in populations GG14 (frequency = 0·017) and ME2 (frequency = 0·2) (Table 4). Several other alleles were specific for single taxa, mostly at low frequencies (Table 4), although not present in all of its populations.


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  		Table 4. Summary of distribution in taxa and populations of alleles with informative distributions
 
The combinations of the most frequent alleles at the other loci were different for groups of taxa, allowing comparison between them. IDH-1 was shared by A. meonanthum and A. braun-blanquetii as the most frequent (sometimes fixed) allele, whereas IDH-2 was the most frequent allele in all other taxa. Six alleles were present in single taxa (Table 4), with low frequencies in some but not all the populations. Among them ACO1-2 stands out because it was the only allele fixed and specific to A. braun-blanquetii. The remaining alleles were shared by two (ACO1-2, AAT1-4, MNR2-2, PGI2-1 and PGM2-6) or three taxa (DIA1-1) (Table 4).

A summary of Nei’s genetic distances, both within and among taxa, is presented in Tables 5 and 6. These values are within the range reported for other Antirrhinum species (Mateu-Andrés, 1999; Mateu-Andrés and Segarra-Moragues, 2000). Within species, mean values of Nei’s distance ranged from 0·003 (A. graniticum ssp. brachycalyx and A. ambiguum) to 0·16 (A. boissieri). The between-species mean values ranged from 0·26 (A. onubensis vs. A. graniticum and A. ambiguum) to 0·40 (A. boissieri vs. all other taxa). The distance between A. meonanthum and A. braun-blanquetii was exceptionally low (0·15), whereas those between A. meonanthum var. rothmaleri and both A. meonanthum var. meonanthum and A. braun-blanquetii were surprisingly high (0·27). The genetic distance between the subspecies of A. graniticum (0·17) was close to the maximum value within species, whereas the distance between A. graniticum ssp. brachycalyx and A. ambiguum was low (0·07).


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  		Table 5. Mean within-taxa Nei’s genetic distances of the studied taxa
 

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  		Table 6. Summary of Nei’s genetic distances between taxa (both average and range are given for each case)
 
The phenograms derived from Nei’s and Rogers’s distances showed high congruence and only the former is shown (Fig. 2). All populations of each taxon appear clustered together without geographic pattern as further explained by Mateu-Andrés and Segarra-Moragues (2003). Two main clusters were found, one comprising A. meonanthum and A. braun-blanquetii, the other comprising the remaining taxa.



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  		Fig. 2. UPGMA clusters derived from Nei’s genetic distance coefficients among the 40 populations studied. Cophenetic correlation is 0·79.

 


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
TAXONOMIC SYNTHESIS FOR THE...
 LITERATURE CITED
 
In both PGI1 and TPI1 different band thicknesses suggested duplicated commigrant loci, so they were not scored. The presence of an extra locus for PGI1 and TPI1 in diploid plants suggests a gene duplication (Gottlieb, 1982), which has been reported in other genera in Antirrhineae (Elisens and Crawford, 1988; Elisens 1992; Elisens and Nelson, 1993) and Antirrhinum (Mateu, 1999; Mateu-Andrés and Segarra-Moragues, 2000).

The allozyme data support the systematic subdivision of the studied taxa into two different groups, Streptosepalum and Antirrhinum. Since not all the taxa included in the second group have been studied, the assignment of rank as subsections (Rothmaler, 1956) or sections (Fernández Casas, 1997) requires more data. In contrast to previous studies, the data presented here do not support the traditional arrangement of species within these groups—subsection Streptosepalum formed by A. meonanthum and A. braun-blanquetii, and subsection Antirrhinum including the remaining taxa, with A. ambiguum being included in A. graniticum.

The genetic distances between the Antirrhinum species studied support the recognition of A. onubensis and A. boissieri at specific rank, both of which have been treated previously as subspecies or varieties of other taxa (Table 1) (Fernández Casas, 1982; Valdés, 1986; Webb, 1971; Sutton, 1988).

Antirrhinum ambiguum shows a closer affinity to A. graniticum than to A. meonanthum, in contrast to previous treatments by Rothmaler (1956) and Fernández Casas (1997), who included it in Streptosepalum with A. meonanthum and A. braun-blanquetii.

Morphological characters including the glandular indumentum and cream (sometimes pink) flower colour (not yellow as stated by Rothmaler) suggest that A. ambiguum is close to A. graniticum. In contrast, A. meonanthum is glabrous and has yellow flowers. The high genetic similarity between A. ambiguum and A. graniticum sensu lato, the morphological characters and the sympatric ranges allow us to consider A. ambiguum as a subspecies of A. graniticum, as A. graniticum Rothm. ssp. ambiguum (Lange) Mateu & Segarra stat. and comb. nov.

The high genetic distance between A. meonanthum var. meonanthum and A. meonanthum var. rothmaleri, is due both to the presence of allele DIA2-1, specific to it, as well as ACO1-3, shared with the A. graniticum group of taxa. These genetic data contrast with the lack of morphological differentiation among A. meonanthum var. meonanthum and A. meonanthum var. rothmaleri, while A. braun-blanquetii, with a lower genetic distance from var. meonanthum, shows clear morphological differences from A. meonanthum. Although these results are in conflict with the existing taxonomy, the lack of morphological differences leads us to maintain A. meonanthum var. rothmaleri at its current rank, pending the collection of the necessary further data to resolve this question. This scenario can be explained by mutation, leading to new alleles, or introgression with one or several other species within its distribution area (as suggested by Webb, 1971), or a combination of both causes.

All the studied species have diagnostic alleles in addition to morphologically distinctive characters. Antirrhinum species are frequently allopatric or parapatric, but sometimes sympatric, although populations of different taxa seldom grow together. Although these Antirrhinum species are fully interfertile (Rothmaler, 1956), pollinators can discriminate between the different species (Mather, 1947), explaining the rarity of natural hybrids. Geographic separation and isolation by distance (Templeton, 1980, 1981; Crawford 1985, 1990) produce a gradual divergence until intrinsic reproductive barriers appear. This fits a geographic pattern of speciation, agreeing with results from Elisens (1992) for Galvezia and Valdés (1970) for Linaria.


   TAXONOMIC SYNTHESIS FOR THE STUDIED TAXA
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 TAXONOMIC SYNTHESIS FOR THE...
LITERATURE CITED
 
Subsection Antirrhinum
Series Hispanica Rothm.

A. graniticum Rothm ssp. graniticum, Bol. Soc. Brot. Ser. 2 13: 279 (1939).

A. graniticum ssp. brachycalyx D.A. Sutton, A revision of the tribe Antirrhineae 83 (1988).

A. graniticum ssp. ambiguum (Lange) Mateu & Segarra, stat. and comb. nov.

Basionym: Antirrhinum ambiguum Lange, Pugillus: 203 (1863).

Synonyms: A. meonanthum var. ambiguum Pau, Fl. Matrit. IX: 88 (1923). A. meonanthum var. glutinosum Reuter, in Wk. Et Lge., Prodr. Fl. Hisp. II: 582 (1870).

A. boissieri Rothm., Feddes Repert. Spec. Nov. Regni Veg. (Beih.) 136: 88 (1956).

Synonyms: A. graniticum Rothm. ssp. boissieri (Rothm.) B. Valdés, Lagascalia 14(1): 91 (1986).

A. onubensis (Fdez. Casas) Fdez. Casas, Fontqueria 15: 39 (1987).

Basionym: Antirrhinum meonanthum ssp. onubensis Fdez. Casas, Fontqueria 2: 27 (1982).

Synonym: A. graniticum Rothm. ssp. onubensis (Fdez. Casas) B. Valdés, Lagascalia 14(1): 91 (1986).

Subsection Streptosepalum Rothm.

Series Meonantha Rothm.

A. braun-blanquetii Rothm., Feddes Repert. 56(3): 280 (1954).

A. meonanthum Hoffmans. & Link var. meonanthum, Fl. Port. 1(9): 261, tab. 51 (1813).

A. meonanthum var. rothmaleri Pinto da Silva, Agronomia Lusitanica 30: 223 (1970).


   ACKNOWLEDGEMENTS
 
We are indebted to C. F. Aguiar, who provided us with seeds of the Portuguese populations of A. braun-blanquetii and A. meonanthum var. rothmaleri, and two reviewers whose comments helped us to improve the work.


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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 TAXONOMIC SYNTHESIS FOR THE...
 LITERATURE CITED
 

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