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A Gene Genealogical Approach to Recognize Phylogenetic Species Boundaries in the Lichenized Fungus Letharia Author(S): Scott Kroken and John W

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A Gene Genealogical Approach to Recognize Phylogenetic Species Boundaries in the Lichenized Fungus Letharia Author(S): Scott Kroken and John W Mycological Society of America A Gene Genealogical Approach to Recognize Phylogenetic Species Boundaries in the Lichenized Fungus Letharia Author(s): Scott Kroken and John W. Taylor Source: Mycologia, Vol. 93, No. 1 (Jan. - Feb., 2001), pp. 38-53 Published by: Mycological Society of America Stable URL: http://www.jstor.org/stable/3761604 . Accessed: 19/07/2011 18:37 Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. 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Mycological Society of America is collaborating with JSTOR to digitize, preserve and extend access to Mycologia. http://www.jstor.org Mycologia, 93(1), 2001, pp. 38-53. ? 2001 by The Mycological Society of America, Lawrence, KS 66044-8897 A gene genealogical approach to recognize phylogenetic species boundaries in the lichenized fungus Letharia Scott Kroken' (Nutt.) Thomson always produce sexual structures John W. Taylor (apothecia). Some individuals also produce clonal Departmentof Plant and MicrobialBiology, 321 symbiotic propagules in the form of isidia, short lat- KoshlandHall, Universityof California,Berkeley, eral branches that break off easily for wind dispersal. USA 94720-3102 California, Mature individuals of Letharia vulpina (L.) Hue rare- ly produce apothecia, whereas all individuals produce clonal propagules in the form of soredia consisting Abstract: Letharia, a of lichenized de- genus fungi of ecorticate wefts of fungal hyphae, each surround- scribed as a of one pair sympatric species, making ing a nest of algal cells. abundant sexual structures and the other making The existence of lichen has been in species pairs few, was investigated as a model system which to called into and it has been that boundaries. Gene of 6 question, proposed recognize species genealogies the clonal lichens are asexual individuals and 12 loci were used to estimate the repeatedly evolutionary from within a sexual (Tehler 1982). of based on the of arising species history Letharia, principles lineage This alternative is of alleles in after hypothesis represented diagram- sorting divergent lineages genetic clonal individuals intermixed isolation. Instead of a of a matically by showing species pair consisting pu- with sexual individuals the tative clonal derived from a sexual throughout phylogeny, species progenitor rather than all the clonal individuals as a Letharia at least six showing species, comprises phylogenetic The between the of single lineage (FIG. 1). disagreement species. Judging by presence perennial apo- Poelt and Tehler turns on whether the sorediate in- thecia and clonal reproductive structures, one spe- dividuals of a species pair represent a separate species cies is exclusively sexual, three species are sexual and or are conspecific with apotheciate forms (Mattsson isidiate, and two species are sorediate and rarely sex- and Lumbsch 1989). We wanted to know whether ual. Not all of these species would have been detect- Letharia vulpina is a phylogenetic or ed with a single gene genealogy, demonstrating the species merely a collection of individuals of Leth- need for multiple independent loci in phylogenetic rarely apotheciate aria columbiana. analysis to recognize recent speciation events. The Until in most results are concordant with aspects of both biological very recently, species recognition lichenized was based on chem- and phylogenetic species recognition. However, only fungi morphological, ical and characters (Purvis 1997). Re- phylogenetic species recognition can be applied to biogeographic cent molecular studies have been based on fungi like Letharia species that are difficult to culti- published vate and mate in the lab. a single locus, usually ITS (e.g., Groner and LaGreca Lohtander et al Thell and Miao Key Words: clonal lichens, coalescence, congru- 1997, 1998a, b, a locus will not re- ence, cryptic species, Lecanorales, metaphyletic spe- 1998). However, single separate if the tree does cies, multiple loci, Parmeliaceae, sibling species, spe- cently diverged species single gene not reflect the and Wollen- cies pair, sympatry species phylogeny (Avise berg 1997, Maddison 1997). FIGURE 2 shows an an- cestral species with two alleles (black and gray) for one locus. Genetic isolation results in two descendant INTRODUCTION species, both of which have inherited the two alleles. The lichenized fungus Letharia was chosen as a mod- The process of lineage sorting eventually results in el genus to investigate species boundaries. Letharia coalescence for one allele in first in species Y, and has been thought to represent a classic example of a then the other in species X. Only when coalescence lichen species pair, defined as one progenitor sexual has occurred for different alleles between the two species and one descendant clonal species (Poelt species can a single locus be used to separate species, 1970, 1972). Mature individuals of L. columbiana and it cannot be known a priori if this has indeed occurred. If phylogenetic species recognition (PSR) Accepted for publication August 18, 2000. were applied before coalescence occurred in both Email: [email protected] species, it would erroneously group the individuals 38 .. n - - -~~~~ KROKEN AND TAYLOR: SPECIES BOUNDARIES IN LETHARIA 39 " ancestral species 1 1 Y Ii. I 4I YI I I V * I I _ | mutation creates two alleles polyphyleticorigins of clonal individuals(Tehler 1982) genetic isolation Ii no coalescence 5 0. L .. coalescence in ] I one species monophyleticorigin of clonal individuals(Poelt 1972) coalescence in / both FIG. 1. Alternate hypotheses of the origin of clonal li- species chens from a sexual species. species X species Y FIG. 2. Lineage sorting for a single locus (after Maddi- containing the black allele or the grey allele as two son and Avise). separate clades and rank them as species. The two described species of Letharia are sympat- sensus approach requires reciprocal fixation (exclu- ric, so there is the possibility of interbreeding. Re- sive sets of alleles) for all loci between the two species productive isolation cannot be determined in lich- (Baum and Shaw 1995). Exclusivity is too strict a cri- enized fungi by the inability to interbreed, because, terion given the long time interval between the be- like many nonlichenized fungi, they have not yet ginning of genetic isolation and reciprocal fixation been crossed in laboratory conditions. However, find- at all loci within those species. A combined analysis ing breeding compatibility would only demonstrate is more sensitive to uncovering recent phylogenetic what can happen in vitro, and not what occurs in divergences, and has uncovered morphologically natural populations. Genetic isolation typically pre- cryptic species in Coccidioidesimmitis (Koufopanou et cedes the development of reproductive barriers, re- al 1997, 1998), Aspergillusflavus (Geiser et al 1998a, sulting in the delimitation of paraphyletic lineages b), and Histoplasma capsulatum (Kasuga et al 1999). larger than actual interbreeding species (Rosen In this study, 12 loci were characterized, and the con- 1979). Therefore, in order to determine breeding gruence of their genealogies was used to recognize barriers in natural populations, we used a PSR based phylogenetic species in Letharia. on the congruence of multiple gene genealogies to group genetically isolated clades that are ranked as phylogenetic species (Taylor et al 1999, 2000). FIG- MATERIALS AND METHODS URE 3 summarizes this with a ex- approach simplified Lichen collection and thalli were col- of recent isolation and line- preparation.-Letharia ample genetic ongoing lected in North America, from California to British Colum- for three loci between two age sorting species. bia, and in Sweden and Italy. Collection information for No single gene genealogy reflects the species phy- Letharia is listed in TABLE I. Lichen thalli were removed logeny, because no locus has completed the process from their substrate (usually conifer bark) and the limits of of lineage sorting for both species. Locus 1 has coa- individuals were identified by locating their holdfasts. From lesced in species X, locus 2 has coalesced in species each thallus, a -10-mg branch was selected for DNA ex- Y, and locus 3 has coalesced in neither species. How- two ever, a combined 3-locus analysis will delimit spe- single gene genealogies combined 3-locus cies, as each branch is supported by two characters. locus 1 locus 2 locus 3 phylogeny For example, species X is supported by allele a-b-c a a- i from locus 1, and allele f-b-c from locus 3 (the rib b b species X c --abs branch to individual 'a' in the combined phylogeny f ed1d d is scored as a homoplastic reversal.) In contrast, a e e e 'Le speciesY f f a f strict consensus of the three single locus genealogies would not detect two species, as the result would be FIG. 3. Three single-gene genealogies, and the congru- an unresolved tree (Barrett et al 1991). A strict con- ence of their gene genealogies. 40 MYCOLOGIA TABLEI. Letharia specimens ID Locationa and date Collector Letharia 'lupina' AP1 USA. WA: Armstrong Peak, Pasayten Wilderness, 7-1997 S. Kroken BC1 CANADA. British Columbia (mycobiont culture) Y Yamamoto CL1 USA.
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