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Department of Plant and Microbial Biology, University of California, Berkeley, California, 94720
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Previous observations of morphological, reproductive and genetic variation have suggested that Neurospora discreta, as presently circumscribed, might represent a diverse complex of multiple species. To investigate this hypothesis we examined the phylogenetic relationships among 73 fungal strains traditionally identified as N. discreta. Strains were chosen from across the morphological, ecological and geographical ranges of the species. Sequence data were obtained from three unlinked nuclear loci, and phylogenetic species recognition was applied to the dataset using protocols that have been shown to be reliable for identifying independent lineages and delineating species of Neurospora. The results demonstrate that the present circumscription of N. discreta includes at least eight separate phylogenetic species. This research also reveals an abundance of previously unrecognized genetic diversity within the genus, characterizes the interspecific evolutionary relationships and contributes to a fuller understanding of species diversity in Neurospora.
Key words: genealogical concordance, phylogenetic species recognition, phylogeny
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, Perkins and Turner 1988, Turner et al 2001, Jacobson et al 2004, Jacobson et al 2005). N. discreta is commonly encountered across the latitudinal and longitudinal range of the genus, making it the most broadly distributed Neurospora species. In the forests of western North America, N. discreta is the most abundant species, accounting for 95% of the isolates collected (Jacobson et al 2004).
A number of observations suggest that N. discreta, as presently circumscribed, might represent a diverse complex of several species. First, strains are distinctly variable in colony morphology when cultured in the laboratory. In addition, conidial pigmentation ranges from yellow to the typical Neurospora orange to a paler and more pink color (Perkins and Raju 1986, Jacobson pers obs). When N. discreta was first described, Perkins and Raju (1986) reported variation in ascospore morphology among crosses. Most Neurospora crosses produce longitudinally ribbed ascospores, but some crosses of N. discreta strains produce ribbed ascospores with slight pits or indentations. Second, inconsistency of sexual fertility in pairings among N. discreta strains is suggestive of a species complex: Some pairs of strains mate well whereas other pairs mate poorly (Perkins and Raju 1986, Jacobson pers obs). This pattern of reproductive compatibility is rare in other biological species (Turner et al 2001, Dettman et al 2003b) and has been observed, to a much lesser degree, only in N. intermedia. Third, abundant genetic diversity was found within N. discreta. In a phylogenetic study of outbreeding species of Neurospora (Dettman et al 2003a) the genetic distances between some N. discreta strains were greater than the genetic distances among other recognized Neurospora species.
In this report we assess the phylogenetic relationships among 73 fungal strains traditionally identified as N. discreta. Strains were chosen to represent the full morphological, ecological and geographical ranges of the species. Sequence data were obtained from three unlinked nuclear loci and analyzed with parsimony and Bayesian phylogenetic methods. To the dataset we applied previously described protocols for phylogenetic species recognition (PSR) that have been shown to be consistent with biological species recognition in Neurospora and, therefore, reliable for identifying independent lineages and delineating species in this genus (Dettman et al 2003a, b). By extending our studies of PSR to N. discreta we confirm the prediction that the present circumscription of N. discreta includes several separate phylogenetic species. The acknowledgment of this complex of multiple species provides an explanation for the aforementioned observations of morphological, reproductive and genetic variation. In addition this research reveals a wealth of previously unrecognized genetic diversity within the genus, contributes to a fuller understanding of species diversity in Neurospora and characterizes the evolutionary relationships among the species. This information is essential to comparative biology and should enhance the utility of Neurospora as an evolutionary model system.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) were collected, cultured and stored following standard protocols (Perkins et al 1976, Jacobson et al 2004). These strains were assigned to N. discreta because they produced more than 50% black ascospores when crossed with N. discreta species testers or because they mated more successfully with N. discreta testers than with any other species testers. Each strain, whether received from a culture collection or collected from the wild, was purified by single conidium subculture to ensure characterization of individual haploid genotypes. Each resulting culture was given a unique identification number starting with "D". The collection of single-conidium strains was redeposited in the FGSC and assigned new FGSC numbers (TABLE I). The N. discreta strains used in Dettman et al (2003a) were included in the present study.
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; Dettman et al 2001, 2003a; Cai et al 2006) have demonstrated that outbreeding Neurospora species collectively form a well supported monophyletic clade. Homothallic Neurospora species are not considered here.
Loci.— –
Sequence data from three unlinked nuclear loci were obtained from the sample of strains. The three microsatellite-containing loci, named DMG, TMI and TML, were characterized in a phylogenetic study by Dettman et al (2003a), which should be consulted for locus information, PCR amplification conditions and sequencing protocols. Previously determined sequences are available from TreeBASE accession M1574, whereas new TMI, DMG and TML sequences have been deposited respectively in GenBank under accession numbers DQ314301
[GenBank]
-314362, DQ314363
[GenBank]
-314427 and DQ314428
[GenBank]
-314490.
Phylogenetic analyses.— – Due to the presence of micro-satellites and insertion/deletion gaps (indels), DNA sequences were aligned manually. Regions of ambiguous alignment and the microsatellite repeats themselves were excluded from phylogenetic analyses. However unambiguously alignable indels and substitution mutations within the microsatellite repeat arrays were phylogenetically informative, so they were coded as multistate characters and included in phylogenetic analyses.
For rooting purposes and genetic distance calculations, exemplar sequences from the seven other outbreeding Neurospora species were included. Species and strain numbers were: N. crassa subgroup NcA, D143; Phylogenetic Species 3, D74; N. intermedia subgroup NiA, D47; Phylogenetic Species 2, D120; Phylogenetic Species 1, D55; N. sitophila, D53, and N. tetrasperma, D145 (see Dettman et al 2003a, b for species designations). These sequence data are available from TreeBASE accession M1574. Unless otherwise stated, sequences from N. crassa D143 (FGSC 2489) were used as outgroup during phylogenetic analyses. Reported genetic distances are Kimura 2-parameter distances.
To avoid confinement at local optima in maximum parsimony (MP) searches, 10 replicates of random stepwise-addition heuristic searches (tree bisection-reconnection branch swapping; maximum of 5000 trees retained [MAXTREES]) were performed with PAUP (version 4.0b8a, Swofford 2001). When multiple MP trees were produced, the tree chosen for display in a figure was the one determined to be most likely using substitution models suggested by Modeltest (version 3.06, Posada and Crandall 1998). Weighted MP heuristic searches had characters weighted inversely proportional to the total number of phylogenetically informative sites contributed by the locus from which they came (relative weights: DMG = 1.00, TMI = 0.64, TML = 0.30). MP bootstrapping was performed with heuristic searches (100 replicates for individual loci, 300 replicates for combined analysis; simple stepwise addition; nearest neighbor interchange branch swapping [NNI]; MAXTREES = 5 000).
Combinability of single-locus datasets was determined by partition homogeneity tests using informative characters and random stepwise-addition MP heuristic searches with 1000 replicates (NNI; MAXTREES = 500). The null hypothesis of congruence was rejected if p < 0.001 (Cunningham 1997). These tests were conservative because all taxa were included, which allows for detection of incongruence both among and within clades.
Bayesian analyses were performed (MrBayes version 3.0b4, Huelsenbeck and Ronquist 2001) as an alternative to the more computationally intensive maximum likelihood analyses. To avoid over parameterization the predetermined likelihood models were used for Bayesian analyses. For example, gamma distributed site-to-site rate variation was implemented only if recommended by Modeltest. Each run consisted of three incrementally heated Markov chains run simultaneously, with default heating values and uniform priors. Markov chains were initiated from a random tree, run for 1 000 000 generations, and sampled every 200th generation. Samples taken before burn-in (<100 000 generations, 500 tree burn-in) were discarded and the remaining samples were used to determine posterior probability distributions. Each run was performed at least twice and consensus trees were compared: All replicate runs converged on congruent trees, suggesting entrapment in local optima did not occur.
Species recognition.— –
For phylogenetic species recognition, previously described protocols (Dettman et al 2003a) were applied to the N. discreta dataset. In brief a clade was recognized as an independent evolutionary lineage if it satisfied either of two criteria: (i) genealogical concordance, in which the clade was present in the majority (at least two out of three) of the single-locus genealogies, as revealed by a majority-rule consensus tree; (ii) genealogical nondiscordance, in which the clade was well supported in at least one single-locus genealogy, as judged by both MP bootstrap proportions and Bayesian posterior probabilities, and was not contradicted in any other single-locus genealogy at the same level of support. To identify such clades a tree possessing only branches that received MP bootstrap proportions 
70% and Bayesian posterior probabilities 0.95 was chosen to represent each of the three loci, then a semistrict consensus tree was produced from these three trees. This criterion prohibited poorly supported nonmonophyly at one locus from undermining well supported monophyly at another locus. When deciding which independent evolutionary lineages should be ranked as phylogenetic species, exhaustive subdivision was applied; all individuals had to be placed within a phylogenetic species, and no individuals were to be left unclassified.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The amount and form of molecular variation differed considerably among the three loci. Even when accounting for differences in mean sequence length, the TML locus provided the largest number of informative nucleotide characters. The relative levels of variation among loci observed in the present study corresponded well with those reported from several other species of Neurospora (Dettman et al 2003a), suggesting these three loci have been evolving in a similar fashion across the genus.
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). Several well supported clades appeared in common among the single-locus genealogies.
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, MP tree length = 353 steps, CI = 0.870). Combined analysis was justified because partition homogeneity tests failed to detect significant incongruence in any of the three pairwise comparisons of loci. As expected, most clades supported by single-locus analyses, received even greater support in combined analyses. The three loci contributed different numbers of phylogenetically informative characters and therefore had different amounts of influence on the combined-analysis tree search. To account for these differences a weighted MP heuristic search was performed with characters weighted in inverse proportion to the number of informative sites contributed by the locus from which they came. Weighted MP trees (not shown) revealed the same clades and relationships among clades as the original MP tree (FIG. 2), further demonstrating that the phylogenetic signals from the independent loci were complementary.
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. Bold branches (FIG. 2
) indicate the clades that satisfied either of the two grouping criteria (genealogical concordance or nondiscordance) and thus were identified as independent evolutionary lineages. Triangles at nodes (FIG. 2 indicate the lineages that satisfied the ranking criterion (exhaustive subdivision) and thus were recognized as phylogenetic species.
Eight phylogenetic species were recognized within this group of 73 individuals, all of which originally were assigned to a single species. The two strains collected from Texas are the type strains for N. discreta (Raju and Perkins 1986) and thus form a phylogenetic species that represents N. discreta sensu stricto. The seven newly discovered Neurospora species were named Phylogenetic Species 4, 5, 6, 7, 8, 9 and 10 (PS4 to PS10 respectively), extending the naming convention of Dettman et al (2003a).
Phylogeny of N. discreta species complex.— –
The eight phylogenetic species typically were well supported in each of the single-locus trees (FIG. 1), with no major conflicts over the placement of individuals within species. The phylogenetic relationships among species were similar between the TMI and TML loci, with slight differences from the lower resolution DMG locus. The three-locus combined-analysis tree (FIG. 2) represents the best estimate of the phylogeny of the N. discreta species complex. Most of the internal branches that united multiple species received significant support, providing a relatively well resolved phylogeny.
The root of the N. discreta complex was located in different positions in different phylogenetic analyses. Single-locus trees place the root on the branch between PS9 and PS10, or leading to a member of PS10. The combined-analysis MP tree placed the root on the branch leading to a member of PS10 (D166). When outgroup representation was increased to seven species, the combined-analysis MP tree (and NJ tree) placed the root between PS9 and PS10, consistent with Bayesian analyses. This rooting position received the most support overall and therefore is displayed (FIG. 2).
Genetic diversity.— –
To display the genetic distances among species, a combined-analysis neighbor-joining tree was constructed from examplar sequences from the N. discreta complex and the seven other outbreeding Neurospora species (FIG. 3). The mean genetic distance among phylogenetic species within the N. discreta complex was 0.0269 (SE = 0.0014), whereas the same statistic was 0.0238 (SE = 0.0012) for the other clade of species, which includes N. crassa, N. intermedia, N. tetrasperma, N. sitophila and three recently described phylogenetic species, PS1-PS3. For maximum genetic distance between two phylogenetic species, the values were 0.0407 for the N. discreta complex (PS5 to PS10), and 0.0336 for the other group (PS2 to N. crassa). Thus the N. discreta species complex contains more species (eight) and more genetic diversity than is found in the other major clade of Neurospora species.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, Perkins and Turner 1988, Turner et al 2001) have designated sets of tester strains that represent most of the known biological species. Mating success is assessed by the proportion of progeny that are viable (i.e. black ascospores). If an individual produces more than 50% black ascospores when crossed with a species tester, the individual is considered conspecific with that tester. Rarely an individual will not produce more than 50% black ascospores with any tester; in this case it is assigned to the species with which it mates best. This method has proven quite effective over many decades and thousands of strains (Turner et al 2001, Dettman et al 2003b, Jacobson et al 2004). Based on these traditional mating tests, at the onset of this project, 73 of the Neurospora individuals included in this study were assigned to a single species, N. discreta. By applying phylogenetic species recognition using genealogical concordance, we have identified eight phylogenetic species within this group. One of these phylogenetic species is composed of the reference strains from the original description of N. discreta (Perkins and Raju 1986) and therefore is N. discreta sensu stricto. Species in the N. discreta complex typically were supported by multiple single-locus genealogies and the three genealogies were very similar regarding the relationships among species, with the exception of PS5, PS9, and PS10. The distinction of PS5 from PS4 was significantly supported by one single-locus genealogy (TMI), but the mixing of PS5 within PS4 in DMG and TML genealogies was not significantly supported and therefore cannot override the strong signal from TMI. PS9 and PS10 each were monophyletic in two of three single-locus genealogies, but again support for the nonmonophyletic phylogenies was not significant.
Two subgroups were named within PS4 to highlight their genetic differentiation, which was apparent at all three loci. These two subgroups, A and B, were not recognized as two phylogenetic species because of the incongruent placement of strains D170 (PS5), D172 (PS5), and D153 (PS4 subgroup A). When PSR was performed with these three strains removed, the two subgroups were recognized as separate phylogenetic species. This result demonstrates how two relatively well differentiated clades linked by a few inconsistently placed strains can be conservatively grouped into one species.
We are not formally naming these newly discovered phylogenetic species at this time because most are composed of a limited number of strains and the patterns of sexual reproductive isolation among species, or compatibility within species, have not yet been characterized. Before naming any species, we want to discover more strains belonging to the smaller species and cross members of the N. discreta complex in a comprehensive fashion to investigate the mating relationships of these species. The information provided by the anecdotal observations of previous mating among strains or with species testers is not sufficient. We will continue to refer to this entire group as the "N. discreta species complex", which is composed of N. discreta sensu stricto and Neurospora Phylogenetic Species 4–10. Taxonomies with arbitrarily named fungal species are common (e.g. O’Donnell et al 2000a, Steenkamp et al 2002, Chaverri et al 2003, Rehner and Buckley 2005) and let researchers communicate effectively before the formal species nomenclature is settled. The point to emphasize is that major phylogenetic divisions are clearly present within the N. discreta complex, and that these divisions are as great as or greater than those among named species such as N. crassa, N. intermedia, N. sitophila and N. tetrasperma.
The phylogeny of N. discreta species complex was generally well resolved, with most internal branches receiving significant support in combined analyses (FIG. 2). The members of species, or terminal clades within species, tended to originate from the same geographic region. For example, PS6 and PS7 were composed respectively of strains from the Ivory Coast and the Caribbean Basin. However the relationship of some species in this complex to geography is not simple, as demonstrated by the range of origins of PS4 strains (Asia, Europe, Africa and North America) and the fact that strains collected from the Ivory Coast could belong to any of three species. When comparing samples collected in North America, a notable phylogeographic division was observed between strains from temperate western North America and those from the tropical Caribbean Basin. In fact western North American strains were consistently more closely related to strains collected from Europe. This same phylogeographic pattern was observed in N. crassa (Jacobson et al 2004, 2005), suggesting that the effects of geography on population divergence might be similar across multiple species of Neurospora.
The discovery of multiple species within the originally described N. discreta, and the understanding of the phylogenetic relationships among species, allows for the reconciliation of several previous observations of reproductive, morphological, and genetic diversity:
(i) Low internal consistency of mating success.— –
Some pairs of strains identified traditionally as N. discreta mate well, whereas other pairs mate poorly ( Jacobson, pers obs). This pattern likely represents mating between conspecific or heterospecific strains, respectively, a distinction that could not be made before our phylogenetic analyses. In some cases an individual was placed within N. discreta because it mated more successfully with the N. discreta tester than with any other species tester, despite never satisfying the 50% black ascospore criterion with any species tester. When Perkins and Raju (1986) described the species, they reported that strains from Florida and Guatemala mated well with the species testers and could be confidently assigned to N. discreta. These three strains (D149, D150 and D151 in this study) belong to PS7, which is closely related to the species testers themselves. In contrast strains from Papua New Guinea (D5 and D148) and New Zealand were not fully fertile with the testers and their assignment to N. discreta was provisional. Strains from Papua New Guinea and New Zealand are phylogenetically placed with PS4 subgroup A, PS9 or PS10, which are more distantly related to the species testers than PS7.
These anecdotal observations on a limited number of matings suggest that strains most closely related to the N. discreta testers are likely to be most sexually compatible with them. Therefore it is likely that many strains originally were described as N. discreta simply because they were more closely related to N. discreta sensu stricto than to any other species known to exist at the time of identification. This pattern is consistent with the positive correlation between phylogenetic divergence and reproductive isolation clearly demonstrated in other Neurospora species (Dettman et al 2003b). We did not cross strains of the N. discreta complex in a systematic manner, so a rigorous comparison of phylogenetic divergence and reproductive isolation could not be made. However the occurrence of different phylogenetic species in sympatry (e.g. PS4–PS6 from the Ivory Coast) indicates that barriers to mating in nature are prevalent enough to maintain the distinctness of species.
(ii) Morphological diversity.— –
Clear morphological differences have been observed among strains assigned to N. discreta. Perkins and Raju (1986) noted that the species testers differed markedly from other strains in macroconidial pigmentation, protoperithecial production and ascospore ornamentation and size. Because Perkins and Raju actually were working with at least four phylogenetic species when N. discreta was described, this variation might represent variation among phylogenetic species within the N. discreta complex. We compared macroconidial pigmentation and colony morphology from a subsample of 44 strains, including representatives from all eight phylogenetic species. Differences in pigmentation and morphology were evident, however they were not consistently species-specific and in some cases variation could be just as great within species as between species (data not shown). In addition, although the extremes of conidial morphology were apparent, the slight gradations along the spectrum of macroconidial morphology were not easily quantified in a reliable manner. Other recent studies in filamentous Ascomycetes also have demonstrated that morphological characters may possess limited taxonomic utility (e.g. O’Donnell et al 2004, Rehner and Buckley 2005) or no phylogenetic information (e.g. Steenkamp et al 2002, Chaverri et al 2003). We do not know if protoperithecial production, ascospore ornamentation or ascospore size track the phylogeny of the N. discreta complex better than macroconidial pigmentation because these characters were not investigated.
Regarding ecological diversity, the N. discreta strains from western North America and southern Europe were collected exclusively from burnt woody shrubs and trees. In contrast, other strains from tropical or subtropical regions were sampled from a variety of substrates, including burned grasses, herbaceous plants, shrubs, twigs and soil (Turner et al 2001). The western North American and European strains formed three minor clades within PS4 subgroup B, but they were not significantly differentiated from other strains within the subgroup. Thus no clear evidence for clade-specific ecological specialization or habitat preference was found.
(iii) Genetic diversity.— –
A previous phylogenetic study of Neurospora (Dettman et al 2003a) showed that N. discreta, despite a small sample size, contained well supported internal subdivisions and high genetic diversity relative to other species. No known characteristics of N. discreta could explain such diversity. With sample size increased to 73 strains, the phylogenetic analyses presented here confirm the high diversity and demonstrate that it is a result of variation among multiple rather than a single species. Although the N. discreta species complex contains more genetic diversity than the other seven outbreeding species combined (FIG. 3), genetic variation within species is similar across the genus (Dettman et al 2003a).
This study demonstrates the power of phylogenetic species recognition to reveal cryptic diversity that may be missed by traditional methods of biological species recognition. Similar conclusions have been drawn in a number of fungal groups (e.g. Vilgalys and Sun 1994, Hibbett et al 1995, Aanen et al 2000, O’Donnell et al 2000b, Taylor et al 2000, Harrington et al 2002, Dettman et al 2003b). An even larger number of studies have shown that multiple, well differentiated phylogenetic species may display little or no distinguishing morphological variation among them (e.g. O’Donnell et al 2004, Rehner and Buckley 2005). Typically, morphological character states are shared among species or have overlapping ranges, rendering them useless for species diagnosis (e.g. Steenkamp et al 2002, Chaverri et al 2003). Because morphological and biological species recognition are not applicable to all organisms, and phylogenetic species recognition appears to be the most effective method for revealing species diversity, many authors are choosing to include information on fixed nucleotide differences in formal species descriptions (Fisher et al 2002, O’Donnell et al 2004).
Since the species’ description in 1986 (Perkins and Raju 1986) only a single paper focusing mainly on N. discreta has been published (Jacobson et al 2004). That study expanded our knowledge of the incidence, distribution and ecology of N. discreta. The present study expands our knowledge of the genetic and species diversity within the N. discreta complex and how it relates to the other Neurospora species. Over the past two years, N. discreta has developed from a rarely collected species believed to be confined to moist tropical and subtropical regions into a common, globally distributed, highly diverse species complex that represents the majority of known diversity in this well studied fungal genus.
Just as more strains must be collected and studied before species can be named, more will be needed before questions can be addressed regarding the biogeography of N. discreta and PS4–PS10. For example, did the entire species complex originate in the southern hemisphere, and are central Africa and the Caribbean present-day centers of diversity? The one clade with the most individuals, PS4 subgroup B, is also the one with the greatest latitudinal distribution of any Neurospora species, from central Africa (Ivory Coast, Gabon, Congo), through Europe and western North America, as far north as Alaska. Studies of potential adaptation of these strains to different environmental parameters might be as productive as those of Drosophila (Oakeshott et al 1982, Loeschcke et al 2000, Ayrinhac et al 2004, Sezgin et al 2004) or other animals (Bradshaw et al 2000, Palo et al 2003, Lindgren and Laurila 2005, Mathias et al 2005), which have been studied along smaller latitudinal gradients.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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1 Corresponding Author. Present address: Department of Botany, University of Toronto, Mississauga, Ontario, L5L 1C6 Canada. E-mail: jdettman{at}utm.utoronto.ca
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  S. W. Peterson Phylogenetic analysis of Aspergillus species using DNA sequences from four loci Mycologia, March 1, 2008; 100(2): 205 - 226. [Abstract] [Full Text] [PDF]
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 M. Karlsson, K. Nygren, and H. Johannesson The Evolution of the Pheromonal Signal System and Its Potential Role for Reproductive Isolation in Heterothallic Neurospora Mol. Biol. Evol., January 1, 2008; 25(1): 168 - 178. [Abstract] [Full Text] [PDF]
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 D.M. Geiser, M.A. Klich, J.C. Frisvad, S.W. Peterson, J. Varga, and R.A. Samson The current status of species recognition and identification in Aspergillus. Stud Mycol, January 1, 2007; 59: 1 - 10. [Abstract] [Full Text] [PDF]
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