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Pollen Dispersal and Interspecific Gene Flow in Louisiana Irises

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Pollen Dispersal and Interspecific Gene Flow in Louisiana Irises Heredity 68 (1992) 399—404 Received 26Apr11 1991 OThe Genetical Society of Great Britain Pollen dispersal and interspecific gene flow in Louisiana irises M. L. ARNOLD*, J. J. ROBINSON, C. M. BUCKNER & B. D. BENNETt Department of Genetics, University of Georgia, Athens, GA 30602, USA An analysis of chloroplast DNA (cpDNA) variation was carried out for 106 individual plants from three natural populations of Louisiana irises. Two of the samples (59 individuals) represented I. brevicaulis populations. The third sample was from a population defined by allozyme markers as an area of contact between I. fidva, I. hexagona and I. brevicaulis. The cpDNA acts as a seed-specific genetic marker because it is inherited from the maternal parent. cpDNA markers were thus used to discriminate between (i) introgressive hybridization due to seed movement followed by pollen transfer and, (ii) introgression resulting from direct transfer of pollen between allopatric populations of the hybridizing taxa. Furthermore, the concurrent analysis of biparental and maternal markers for the same individuals allowed a test for any directionality in the introgression. A comparison of cpDNA results with data from previous nuclear analyses led to the conclusion that pollen flow occurred from allopatric populations of I. hexagona into an area of sympatry involving I. fulva and I. brevicaulis. In addition, the genotypes detected in the hybrid population indicate that 1. fulva and I. brevicaulis have acted as both pollen and seed parents to produce introgressant individuals. The results of the present study and those of previous nuclear and cpDNA analyses suggest that pollen dispersal is the most important avenue for gene flow between these Iris species. Keywords:chioroplastDNA, introgression, Iris, plants. Introduction patric populations of the hybridizing taxa. The mechanism of interspecific gene flow may have a signi- Oneaspect of gene flow in plants, suggested as a major ficant impact on the pattern and extent of dispersal stimulus for evolution, involves the transfer of genetic and, thus, the genetic structure of areas of overlap material between hybridizing taxa (i.e. introgression; (Barton & Hewitt, 1985; Asmussen et at., 1989). Anderson, 1949). The process of introgressive hybrid- Furthermore, the avenue of gene flow between hybrid- ization, like gene flow in general, may act to restrain izing taxa should either enhance or decrease the likeli- evolution by leading to the amalgamation of the hood of allopatric introgression (Potts & Reid, 1988; hybridizing taxa (Grant, 1963). Alternatively, intro- dePamphilis & Wyatt, 1989; 1990; Arnold eta!., 1990 gression may be evolutionarily creative by facilitating a,b; 1991). (i) an increase in the fitness of the introgressed form A classic example of introgressive hybridization (Nagle & Mettler, 1969; Bennett, 1989; Bennett & involves species from the 'Louisiana Iris' group Grace, 1990), (ii) an invasioit of extreme environments (Anderson, 1949). Some of the species in this complex by the introgressed form (Lewontin & Birch, 1966, but have geographical ranges that are closely associated see Gibbs, 1968 and Birch & Vogt, 1970) and/or (iii) with the Mississippi drainage (I. fulva and 1. brevicaulis), the process of speciation (Mecham, 1960; Levin, 1969; while others are associated with freshwater marsh Rieseberg et a!., 1990). In plants, the first phase of habitats extending from Texas to South Carolina (1. introgressive hybridization may be accomplished by hexagona; Randolph et a!., 1967; Bennett, 1989; N. seed dispersal into populations of the alternate taxon Henderson, personal communication). The habitats followed by pollen transfer (sympatric introgression) associated with each species include moist hardwood or, alternatively, by the transfer of pollen between allo- forests (1. brevicaulis), understory regions along the banks of bayous derived from the Mississippi river (I. *Correspondence tPresent address: Espey, Huston & Associates, Inc., 888 West Belt fulva) and open freshwater marshes (I. hexagona; Dr. South, Suite 200, Houston, TX 77042, USA. Viosca, 1935; Bennett, 1989). The area of geograph- 399 400 M. L. ARNOLD ETAL. ical overlap between these three species occurs in there are habitats typically occupied by either I. fu!va southern Louisiana and numerous cases of natural or I. hexagona within a few kilometres of the hybrid hybridization have been reported from this region population. (Viosca, 1935; Riley, 1938; Anderson, 1949; DNA isolation was carried out using leaf material Randolph eta!.1967;Bennett & Grace, 1989; Arnold and the procedure described by Arnold et a!. (1990b). et a!., 1 990a, b; 1991). Recent studies of this species This resulted in the collection of both nuclear and complex have determined the distribution of nuclear, cytoplasmic DNA. The identification of diagnostic genetic markers and have led to the inference of both cpDNA markers for I. brevicaulis, I. fulva and I. sympatric and allopatric introgression (Arnold et a!., hexagona involved the use of oligonucleotide primers 1 990a, b; 1991). An initial study of chloroplast DNA that were designed to anneal to the region containing (cpDNA) markers for I. fu!va and I. hexagona the ribulose-1, 5-bisphosphate carboxylase gene (i.e. suggested that introgression between these two species rbcl; Z 1, 5'-ATGTCACCACAAACAGAAACTAA- was a result of pollen being transferred between allo- AGCAAGT-3', McIntosh et a!., 1980; ORF1O6, 5'- patric populations of the taxa rather than seed disper- ACTACAGATCTCATACTACCCC-3', Hiratsuka et sal followed by pollen transfer (Arnold et a!., 1991). A a!., 1989). The Zi primer shares sequence identity test for the mechanism of gene flow between these two with the Zea mays rbc! gene from positions 1—30 species was possible because the cpDNA markers are (Mcintosh et a!., 1980). The ORF1O6 primer shares maternally inherited and, therefore, act as seed-specific sequence identity with the Oryza sativa conserved open markers (Arnold et a!., 1991). We have extended our reading frame region, ORF1O6 (Hiratsuka et a!., 1989). analysis of gene flow between iris species by examining PCR amplification of this cpDNA region was accom- cpDNA variation in populations of I. brevicaulis and in plished using the following protocol: Reaction a population containing nuclear markers characteristic volume 100 p1; reaction mix 10 mtvi Tris-HC1 (pH of I. brevicau!is, I. hexagona and I. fulva. These data 8.3), 50 mi KC1, 1.5 mtvi MgCl7, 0.001% gelatin, 0.1 were used to test for the presence of maternal lineages mM each of dATP, TTP, dCTP and dGTP, 50 pmol of originating from these three species. By comparing each primer, 1—2 g of genomic DNA and 2.5 units of data for biparentally transmitted nuclear markers Taq DNA polymerase (Perkin Elmer Cetus). The (Arnold et a!., 1990a, b; 1991) with the maternally amplification experiments were carried out using a transmitted cpDNA markers, we were able to test for Perkin Elmer Cetus DNA Thermal Cycler. The ther- introgression resulting from pollen flow between allo- mal cycler was programmed for one cycle of 1 mm at patric populations versus introgression due to seed dis- 94°C, 35 cycles of 1 mm at 94°C, 1 mm at either 55°C persal into populations of the alternate species, or 60°C, 4 min at 72°C and one cycle of 7 mm at 72°C. followed by pollen transfer. It was also possible to test The cpDNA amplification products were used in res- for any restriction on which species may act as the triction endonuclease digests to identify diagnostic res- maternal parent in interspecific crosses. triction site or length differences. Initial digests to identify diagnostic markers for I. Materialsand methods brevicau!is, I. fu!va and I. hexagona involved 10 enzymes (HphI, A!uI, BamHI, BstUl, EcoRI, HaeIII, Atotal of 106 individual iris plants from three popula- HhaI, HindJII, PstI, and RsaI; New England Biolabs). tions were examined for chioroplast DNA markers. The various fragments were resolved using 1.5% These populations include two populations identified agarosegels run at 75 V for approximately 5 h. EtBr as I. brevicaulis, and one population that had allozyme was present in the gels during electrophoresis to allow markers characteristic of I. brevicaulis, 1. fulva and 1. photography of the restriction fragments under ultra- hexagona (Arnold et aL, 1990a). The collection locali- violet light. ties for these populations are the following ('n' sample sizes): I. brevicaulis; Louisiana, St. Martin Results Parish, St. Martinville, n =20;Ascension Parish, Prairieville, n =39;Hybrid Popu!ation; Louisiana, St. Figure1 illustrates both restriction site and length var- Martin Parish, St Martinville, n =47.The hybrid iation between the rbc! amplification products from I. population was estimated to possess hundreds of indi- brevicaulis, 1. fulva and I. hexagona. Amplification of vidual plants and extends semicontinuously for over 1 this region of cpDNA from I. fulva and I. hexagona km. Populations of I. brevicaulis are known to occur resulted in the production of an approximately 3.2 kb within 5 km of this hybrid population. Populations of fragment (Fig. 1; Arnold et a!., 1991). In contrast, the both I. fulvaandI. hexagona have been sampled within amplification product from this region for I. brevicaulis approximately 70 km of this population. However, individuals was approximately 3.5 kb in length (Fig. 1; INTROGRESSION IN LOUISIANA IRISES 401 abcdefghij abcde fgh ijk Imnopq rs 2.2O 1.60— 1.56— 1.20 — 0.B3 — 0.96— 0.56 — 0.65— 0.37 — 0.47" 0.23 — 0.25' Fig.2 HhaI restriction digests of PCR amplification 0.16" products of the rbcl region from individual iris plants in an area of contact between I. fulva, 1. brevicaulis and!. hexagona. Lane a = phage DNA digested with BstYI; Fig. I PCR amplification products and restriction digests of Lanes b-s contain HhaI digested, amplified DNA from these products from I. fulva, I. brevicaulis and I. hexagona. individual iris plants. Individuals in Lanes b, c, e—g, j,1,m, Lane a =4X174 DNA digested with Rsal; lane b =rbc! q—s have the restriction fragment pattern characteristic of 1.
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