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Brief Communication |
Chaire de recherche du Canada en génomique forestière et environnementale and Centre de recherche en biologie forestière, Pavillon Charles-Eugène Marchand, Université Laval, Sainte-Foy, Québec, Canada G1K 7P4
Received for publication December 3, 2002. Accepted for publication June 20, 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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Key Words: allopatric speciation • genetic diversity • mtDNA • Picea • Pinaceae • progenitor-derivative species pair
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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). Evidence for progenitor-derivative species pairs includes a high degree of genetic similarity between the two taxa, a narrower and ecologically more restricted distribution range, and a lower genetic diversity for the putative derivative species relative to its progenitor (Gottlieb et al., 1985
; Witter, 1990
). Frequently, the two taxa can interbreed to form viable hybrids, and the genetic diversity of the derivative is generally a subset of that observed in the progenitor (Gottlieb et al., 1985
).
Many progenitor-derivative species relationships have been deduced in plants based on ecological and genetic data. Early on, allozyme data were used to recognize the allopatric speciation of single populations of Stephanomeria (Gottlieb, 1973
) and Clarkia (Gottlieb, 1974
). Other taxa such as Layia discoidea and Salix silicola, which appeared to be relics of ancient species because of their narrow distribution and particular morphologies, were later confirmed to originate from related species with wider ecological distributions (e.g., Gottlieb et al., 1985
; Purdy and Bayer, 1995
).
Recently, data derived from nuclear expressed sequence tag polymorphisms (ESTPs) were used to support the hypothesis of a progenitor-derivative species pair between the North American transcontinental black spruce (Picea mariana [Mill.] BSP) and the eastern red spruce (P. rubens Sarg.) (Perron et al., 2000
). Both black spruce and red spruce are characterized by predominantly outcrossing mating systems and low levels of population differentiation (Eckert, 1989
; Hawley and Dehayes, 1994
; Isabel et al., 1995
; Rajora et al., 2000
; Perry and Bousquet, 2001
; Gamache et al., 2003
). Contrary to most boreal conifers including black spruce, red spruce is genetically depauperated and harbors low levels of genetic diversity at allozyme loci (Eckert, 1989
; Hawley and DeHayes, 1994
; Rajora et al., 2000
), randomly amplified polymorphic DNA (RAPD) loci (Perron et al., 1995
) and nuclear gene/ESTP loci (Perron et al., 2000
). In addition, alleles observed at 26 ESTP loci in red spruce were a strict subset of those in black spruce (Perron et al., 2000
), which is strong evidence for progenitor-derivative species relationships (Gottlieb et al., 1985
). At some loci, reversed patterns of allele frequency were observed, suggesting the involvement of genetic drift and allopatric speciation. Genetic drift simulations have further supported the scenario of allopatric speciation, which would have taken place during the second half of the Pleistocene (Perron et al., 2000
). Other ecological (Manley, 1972
; Gordon, 1976
; Bobola et al., 1996
), morphological (Gordon, 1976
; Weng and Jackson, 2000
), biochemical (von Rudloff, 1975
; Chang and Hanover, 1991
), and phylogenetic (Wright, 1955
; Sigurgeirsson and Szmidt, 1993
) evidence, as well as the natural introgressive hybridization previously reported (Morgenstern and Farrar, 1964
; Manley, 1972
; Bobola et al., 1996
; Perron and Bousquet, 1997
; Johnsen et al., 1998
), support a close relationship between black spruce and red spruce.
Cases for progenitor-derivative species pairs are best supported when data from different genomes result in congruent trends (Kadereit et al., 1995
). In the present investigation on the progenitor-derivative relationship between black spruce and red spruce, we have used maternally inherited mitochondrial DNA markers (Jaramillo-Correa et al., 2003
) to complement the information retrieved previously at nuclear gene loci (Perron et al., 2000
). In doing so, we attempt to confirm the trends previously reported and the hypothesis of recent allopatric speciation.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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for details) aimed at comparing the genetic diversity between black spruce and red spruce at the nuclear gene level. Specifically, the same trees from six allopatric populations, three of black spruce (Parc Mistassini, Manicouagan, Ipsala) and three of red spruce (October M.S.F., Glade Run, Indian Cap), were considered for analysis to enable a direct comparison of genetic diversity estimates between nuclear and mitochondrial DNA loci (Table 1). Because of the lack of mtDNA diversity in the three allopatric populations of red spruce above (see Results), two additional populations of red spruce from the area of allopatry were considered to confirm the diversity trend observed (Upper Jay and Bear Meadows) (Table 1). Although not absolute, the delineation of the zones of allopatry followed previously published natural ranges (Blum, 1990
; Viereck and Johnston, 1990
).
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). Of these, six markers were monomorphic among spruce species, and the remaining three loci (SSU rRNA V1 region, nad1 intron b/c, and nad5 intron1) had polymorphisms among spruce taxa and within some of them. These three markers were used in the present study to compare the genetic diversity in mtDNA between black spruce and red spruce. DNA was extracted from needles with a Dneasy Plant Mini Kit (Qiagen, Valencia, California, USA) and amplified in a PTC-225 thermal cycler (MJ Research, Waltham, Massachusetts, USA) using 0.1 µmol/L of each primer, 0.1 mmol/L of each dNTP, 1% (m/v) reaction buffer, 1.5 mmol/L MgCl2, and 0.125 units platinum Taq DNA polymerase (Invitrogen/Applied Biosystems, Foster City, California, USA). The PCR and gel electrophoresis conditions varied from one marker to the next and were set as reported elsewhere (Jaramillo-Correa et al., 2003
).
Estimates of genetic diversity for each population were obtained by considering each locus individually and then by considering simultaneously the genotypes at the three loci to determine mtDNA haplotypes (mitotypes). The percentage of polymorphic loci (Pp) and the mean number of alleles per locus (A) were estimated on a locus basis. The number of mitotypes (nh) and the total mtDNA diversity (H; equivalent to the expected heterozygosity, He, for diploid data; Weir, 1996
) were estimated from mitotype data. The heterogeneity of mitotype frequencies between black spruce and red spruce was tested by using a G test with Williams' correction for small sample sizes (Sokal and Rohlf, 1995
). Differences between species genetic diversity were tested by using a nonparametric Mann-Whitney rank test (Sokal and Rolf, 1995
). Evolutionary relations among mitotypes were deduced using a nested clade analysis following the methods of Templeton et al. (1992)
. The clade was built considering only those indels responsible for the differences between mitotypes. These indels were previously detected by both fragment size analysis on gel electrophoresis and by DNA sequencing (Jaramillo-Correa et al., 2003
). Categorical associations between species and mitotypes were performed following the procedures of Templeton and Sing (1993)
.
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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). Such a trend is expected for a progenitor-derivative species relationship. All three mtDNA marker loci tested were polymorphic in all black spruce populations and monomorphic in the three southernmost populations of red spruce (Fig. 1). In black spruce, two alleles were observed for each of the three mtDNA loci surveyed, and four different mitotypes were detected when considering simultaneously the genotypes at the three loci (Table 1). In red spruce, except for three individuals from the two northernmost provenances (one from the Massachusetts provenance and two from the New York State provenance), populations were fixed for all three mtDNA marker loci and harbored only mitotype IV (Table 1, Fig. 2). None of these alleles and mitotypes was unique to red spruce.
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). In addition, the polymorphisms and mitotypes detected in black spruce and red spruce were not detected in a range of other spruce species, including the sympatric but taxonomically distantly related P. glauca (Jaramillo-Correa et al., 2003
). Differences among haplotypes in black spruce and red spruce were due exclusively to indels; no substitutions or additional polymorphisms were revealed by DNA sequencing. As previously reported (Jaramillo-Correa et al., 2003
), there was a complete linkage between the genes nad1 and nad5 and all possible combinations between these two genes and SSU rRNA were observed.
In the nested clade analysis (Fig. 3), all four mitotypes were interconnected, forming a loop and showing no specific evolutionary trend about the history or origin of any mitotype. When the species level was added into the analysis, haplotypes harbored by red spruce were grouped in clade 1–2, a subsample of the mitotypes present in black spruce, which bore the total clade (Fig. 3). Patterns of genetic diversity observed here at the mtDNA level, together with data from 26 nuclear gene loci (Perron et al., 2000
), provide additional support to the notion that the genetic variation detected in red spruce is a subset of that observed in black spruce. Such a trend is expected for a progenitor-derivative species pair (Gottlieb et al., 1985
).
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Only three individuals from red spruce populations from the states of Massachusetts and New York did not harbor mitotype IV, the mitotype found in the remaining 61 trees of these and other red spruce populations sampled. The presence of mitotype III in these three individuals can be explained in two possible ways. First, similarly as for mitotype IV, mitotype III was maintained in red spruce after speciation (see above), and it could not be detected in southernmost populations because of insufficient sampling or because it was simply lost due to fluctuations in population sizes. Alternately, it is possible that the presence of mitotype III in the northernmost populations of red spruce is the result of recent interspecific gene leakage via hybridization with black spruce, where mitotype III has been more frequently observed. The northernmost populations of red spruce considered here are next to the zone of contact with black spruce, where interspecific gene flow has already been detected with nuclear DNA markers (Bobola et al., 1996
; Perron and Bousquet, 1997
; Perron et al., 2000
).
Given the poor resolution observed in the nested clade analysis (Fig. 3), it is difficult to discern between these two competitive explanations, ancestral polymorphism and recent interspecific gene flow, although the former one appears poorly supported by biogeographical data. Panylogical and paleoecological studies have revealed that during the last glacial maximum, around 18 000 yr BP (see Dyke and Prest, 1987
), species from the genus Picea were confined to glacial refugia in the Great Plains (McLeod and MacDonald, 1997
) and in the southeastern parts of the United States (Davis, 1983a
, b
). Subsequently, spruce species migrated northward. Given such a migration pattern, we would expect to detect mitotype III in the southernmost populations of red spruce if it was ancestral and present in red spruce refugia. But it was not observed, thus lending support for the explanation of recent interspecific gene flow. In any case, a more detailed analysis including additional sampling should help elucidate the question.
It was previously shown through extensive simulation studies that the lower genetic diversity observed in the nuclear genome of allopatric red spruce (a reduction of 32% in the number of alleles per locus and 49% in the expected heterozygosity, as compared to the species base level of allopatric black spruce) could be achieved by genetic drift during 10 000–25 000 generations in an isolated black spruce population that would harbor the current genetic diversity observed in P. mariana and with an effective population size in a range between 10 000 and 25 000 individuals (Perron et al., 2000
). Assuming a generation time of 20 yr, between 200 000 and 500 000 yr would be necessary to reach such a reduction in genetic diversity. Thus, given the succession of quaternary glaciations and short periods of range expansion during unglaciated periods, the divergence between black spruce and red spruce could have well proceeded towards the end of the Pleistocene era (Perron et al., 2000
).
The lack of genetic diversity observed at the mtDNA level in red spruce fits well this scenario of allopatric speciation, but the observed reduction of genetic diversity is more drastic for mtDNA loci than for nuclear gene loci (see above). However, in a monoecious species, one would expect a neutral mitochondrial gene polymorphism to reach fixation two times faster than a nuclear gene in absence of gene flow (Birky et al., 1983
). Given the large reduction in gene diversity already observed at nuclear loci for red spruce (Perron et al., 2000
), it is likely that most of mtDNA diversity found in an isolated ancestral population of black spruce would be lost if a mild bottleneck occurred over a period of 10 000–25 000 generations, as described earlier. On the opposite, given the slow rate of molecular evolution of mtDNA in plants (Laroche et al., 1997
) and conifers in particular (Jaramillo-Correa et al., 2003
), it is unlikely that the genetic diversity in the mtDNA of black spruce would be derived (apomorphic). Rather, it appears to be ancestral.
The previous scenario of allopatric speciation involves the isolation of an ancestral population of black spruce over a long period during one or several glaciations in the Pleistocene. Such isolation in drift-promoting conditions should not only translate into reductions of genetic diversity but also into divergent patterns of allele frequencies at some loci. For nuclear gene loci, allele frequencies between black spruce and red spruce differed significantly for some loci (Perron et al., 2000
). Most often, the common alleles at nuclear ESTP loci in black spruce were fixed or nearly fixed in populations of red spruce, but for some loci, reversed patterns of allele frequencies indicative of genetic drift were observed (Perron et al., 2000
). In the present study, differences in mitotype frequencies between black spruce and red spruce were also significant (G = 48.4; P < 0.001), and reversed patterns of frequencies between the two species were observed. For instance, the most prevalent mtDNA variant in two out of three populations of black spruce, mitotype I, was absent from populations of red spruce (Fig. 2). These patterns suggest that drift-promoting conditions were encountered in the recent past, presumably during a speciation process involving geographic isolation.
Allopatric speciation promoted by geographic isolation is believed to be a dominant force shaping taxonomical diversity in the genus Picea (Wright, 1955
). Biogeographical trends indicate that several pairs of closely related taxa with parapatric or partially overlapping ranges are characterized by weak reproductive isolation; most if not all southern species have smaller geographic ranges and less morphological diversity than northern species (Wright, 1955
). On the other hand, the hypothesis of sympatric speciation could be argued if red spruce had originated through ecological specialization within a marginal black spruce population. However, this possibility is unlikely, considering that black spruce is characterized by an outcrossing mating system and by high levels of gene flow among populations (Govindaraju, 1989
; Isabel et al., 1995
; Perry and Bousquet, 2001
; Gamache et al., 2003
). These life-history traits would counteract the two main conditions for sympatric speciation: habitat-restricted mating and disruptive selection among different habitats (Johnson et al., 1996
). Under these circumstances, we would not expect the neutral genetic diversity of red spruce to be a subset of that observed in black spruce. On the other hand, long-term habitat fragmentation driven by large-scale climatic fluctuations, such as those likely experienced during the Pleistocene by boreal species, must have provided ideal conditions for allopatric speciation (Critchfield, 1984
; Nowak et al., 1994
). Under such circumstances, the action of genetic drift would erode efficiently the genetic diversity over long periods of geographic isolation.
In addition to the genetic evidence from two genomes, the three main criteria for invoking a progenitor-derivative relationship between two taxa (Gottlieb et al., 1985
) are met for the red spruce–black spruce species pair. First, the two taxa can interbreed and form viable hybrids (Wright, 1955
; Morgenstern and Farrar, 1964
; Gordon, 1976
; Perron and Bousquet, 1997
; Johnsen et al., 1998
). Second, the putative derivative species (red spruce) has a narrower natural range and is ecologically more restricted than its transcontinental progenitor (black spruce) (Wright, 1955
; Gordon, 1976
; Blum, 1990
). Third, there is a high degree of genetic similarity between the two taxa (Gordon, 1976
; Sigurgeirsson and Szmidt, 1993
; Perron et al., 1995
, 2000
; Bobola et al., 1996
; present study), and the genetic diversity of the putative derivative species is a subset of that observed in the progenitor (Perron et al., 2000
; Jaramillo-Correa et al., 2003
; present study). Moreover, both species are also difficult to distinguish through morphology (e.g., Wright, 1955
; Weng and Jackson, 2000
) and biochemistry (von Rudloff, 1975
; Chang and Hanover, 1991
), indicating high taxonomic and genetic relatedness. Thus, all published genetic, ecological, morphological, and reproductive evidence concurs to support a progenitor-derivative species relationship between black spruce and red spruce.
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FOOTNOTES |
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2 E-mail: bousquet{at}rsvs.ulaval.ca
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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