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Chromosomal Speciation Revisited: Modes of Diversification in Australian Morabine Grasshoppers (Vandiemenella, viatica Species Group).

Kawakami T, Butlin RK, Cooper SJ - Insects (2011)

Bottom Line: Our population genetic and phylogeographic analyses revealed extensive non-monophyly of chromosomal races along with historical and on-going gene introgression between them.These findings suggest that geographical isolation leading to the fixation of chromosomal variants in different geographic regions, followed by secondary contact, resulted in the present day parapatric distributions of chromosomal races.The significance of chromosomal rearrangements in the diversification of the viatica species group can be explored by comparing patterns of genetic differentiation between rearranged and co-linear parts of the genome.

View Article: PubMed Central - PubMed

Affiliation: Division of Biology, Kansas State University, Manhattan, Kansas 66506, USA. kawakami.t@gmail.com.

ABSTRACT
Chromosomal rearrangements can alter the rate and patterns of gene flow within or between species through a reduction in the fitness of chromosomal hybrids or by reducing recombination rates in rearranged areas of the genome. This concept, together with the observation that many species have structural variation in chromosomes, has led to the theory that the rearrangements may play a direct role in promoting speciation. Australian morabine grasshoppers (genus Vandiemenella, viatica species group) are an excellent model for studying the role of chromosomal rearrangement in speciation because they show extensive chromosomal variation, parapatric distribution patterns, and narrow hybrid zones at their boundaries. This species group stimulated development of one of the classic chromosomal speciation models, the stasipatric speciation model proposed by White in 1968. Our population genetic and phylogeographic analyses revealed extensive non-monophyly of chromosomal races along with historical and on-going gene introgression between them. These findings suggest that geographical isolation leading to the fixation of chromosomal variants in different geographic regions, followed by secondary contact, resulted in the present day parapatric distributions of chromosomal races. The significance of chromosomal rearrangements in the diversification of the viatica species group can be explored by comparing patterns of genetic differentiation between rearranged and co-linear parts of the genome.

No MeSH data available.


Estimated allele frequency clines of chromosomal (dotted red line), nuclear (solid black line) and mitochondrial markers (dashed blue line) across a hybrid zone between P24(XY) (to the left side) and viatica17 (to the right side) on Kangaroo Island based on maximum likelihood models. Best fit models are the sigmoid model for the chromosomal and mitochondrial markers and asymmetrical stepped model for the nuclear markers. Circles, squares, and triangles represent observed allele frequencies of chromosomal, nuclear (average of 10 autosomal loci), and mitochondrial markers, respectively. Distance is expressed relative to the center (= 0 km) of the average nuclear cline.
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f2-insects-02-00049: Estimated allele frequency clines of chromosomal (dotted red line), nuclear (solid black line) and mitochondrial markers (dashed blue line) across a hybrid zone between P24(XY) (to the left side) and viatica17 (to the right side) on Kangaroo Island based on maximum likelihood models. Best fit models are the sigmoid model for the chromosomal and mitochondrial markers and asymmetrical stepped model for the nuclear markers. Circles, squares, and triangles represent observed allele frequencies of chromosomal, nuclear (average of 10 autosomal loci), and mitochondrial markers, respectively. Distance is expressed relative to the center (= 0 km) of the average nuclear cline.

Mentions: A secondary origin of the parapatric distribution is supported by the narrowness of the hybrid zones relative to the dispersal rate of grasshoppers and patterns of gene introgression across a hybrid zone between P24(XY) and viatica17 on Kangaroo Island [29]. Hybrid zone analyses using a maximum-likelihood approach gave an average estimate of cline width w = 310 m and dispersal parameter σ = 48.7 m/generation1/2 for 10 autosomal markers (Figure 2). If the contact zone between these two races had a primary origin > 1.0 million years ago, hybrid zone widths for putatively neutral markers should have been much wider than 310 m. In addition, widths and positions of clines for these ten nuclear markers were concordant and coincident with the chromosomal cline. Such concordant and coincident clines are thought to originate from secondary contact between the chromosomal races or strong linkage between nuclear and chromosomal markers. Although genomic locations of these nuclear markers are unknown, it is unlikely that all ten autosomal markers are located on the rearranged chromosomes (i.e., X chromosome inversion and a fusion between the inverted X chromosome and an acrocentric autosome). In contrast to the nuclear markers, the mitochondrial COI marker showed a significantly wider cline (911 m) with center offset toward the P24(XY) side (409 m). Although there are several mechanisms that could result in the discordance between the mitochondrial and nuclear clines, such as asymmetrical hybridization, differences in fitness, differences in female mate preference and male aggression, hybrid zone movement toward the viatica17 side after secondary contact would be the most likely given the overall asymmetry of the clines in the nuclear markers. The results further suggest that reduction of nuclear gene flow may be associated with the chromosomal variation, or underlying genetic variation linked with chromosomal variation, whereas mtDNA gene flow appeared to be independent of this variation.


Chromosomal Speciation Revisited: Modes of Diversification in Australian Morabine Grasshoppers (Vandiemenella, viatica Species Group).

Kawakami T, Butlin RK, Cooper SJ - Insects (2011)

Estimated allele frequency clines of chromosomal (dotted red line), nuclear (solid black line) and mitochondrial markers (dashed blue line) across a hybrid zone between P24(XY) (to the left side) and viatica17 (to the right side) on Kangaroo Island based on maximum likelihood models. Best fit models are the sigmoid model for the chromosomal and mitochondrial markers and asymmetrical stepped model for the nuclear markers. Circles, squares, and triangles represent observed allele frequencies of chromosomal, nuclear (average of 10 autosomal loci), and mitochondrial markers, respectively. Distance is expressed relative to the center (= 0 km) of the average nuclear cline.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4553423&req=5

f2-insects-02-00049: Estimated allele frequency clines of chromosomal (dotted red line), nuclear (solid black line) and mitochondrial markers (dashed blue line) across a hybrid zone between P24(XY) (to the left side) and viatica17 (to the right side) on Kangaroo Island based on maximum likelihood models. Best fit models are the sigmoid model for the chromosomal and mitochondrial markers and asymmetrical stepped model for the nuclear markers. Circles, squares, and triangles represent observed allele frequencies of chromosomal, nuclear (average of 10 autosomal loci), and mitochondrial markers, respectively. Distance is expressed relative to the center (= 0 km) of the average nuclear cline.
Mentions: A secondary origin of the parapatric distribution is supported by the narrowness of the hybrid zones relative to the dispersal rate of grasshoppers and patterns of gene introgression across a hybrid zone between P24(XY) and viatica17 on Kangaroo Island [29]. Hybrid zone analyses using a maximum-likelihood approach gave an average estimate of cline width w = 310 m and dispersal parameter σ = 48.7 m/generation1/2 for 10 autosomal markers (Figure 2). If the contact zone between these two races had a primary origin > 1.0 million years ago, hybrid zone widths for putatively neutral markers should have been much wider than 310 m. In addition, widths and positions of clines for these ten nuclear markers were concordant and coincident with the chromosomal cline. Such concordant and coincident clines are thought to originate from secondary contact between the chromosomal races or strong linkage between nuclear and chromosomal markers. Although genomic locations of these nuclear markers are unknown, it is unlikely that all ten autosomal markers are located on the rearranged chromosomes (i.e., X chromosome inversion and a fusion between the inverted X chromosome and an acrocentric autosome). In contrast to the nuclear markers, the mitochondrial COI marker showed a significantly wider cline (911 m) with center offset toward the P24(XY) side (409 m). Although there are several mechanisms that could result in the discordance between the mitochondrial and nuclear clines, such as asymmetrical hybridization, differences in fitness, differences in female mate preference and male aggression, hybrid zone movement toward the viatica17 side after secondary contact would be the most likely given the overall asymmetry of the clines in the nuclear markers. The results further suggest that reduction of nuclear gene flow may be associated with the chromosomal variation, or underlying genetic variation linked with chromosomal variation, whereas mtDNA gene flow appeared to be independent of this variation.

Bottom Line: Our population genetic and phylogeographic analyses revealed extensive non-monophyly of chromosomal races along with historical and on-going gene introgression between them.These findings suggest that geographical isolation leading to the fixation of chromosomal variants in different geographic regions, followed by secondary contact, resulted in the present day parapatric distributions of chromosomal races.The significance of chromosomal rearrangements in the diversification of the viatica species group can be explored by comparing patterns of genetic differentiation between rearranged and co-linear parts of the genome.

View Article: PubMed Central - PubMed

Affiliation: Division of Biology, Kansas State University, Manhattan, Kansas 66506, USA. kawakami.t@gmail.com.

ABSTRACT
Chromosomal rearrangements can alter the rate and patterns of gene flow within or between species through a reduction in the fitness of chromosomal hybrids or by reducing recombination rates in rearranged areas of the genome. This concept, together with the observation that many species have structural variation in chromosomes, has led to the theory that the rearrangements may play a direct role in promoting speciation. Australian morabine grasshoppers (genus Vandiemenella, viatica species group) are an excellent model for studying the role of chromosomal rearrangement in speciation because they show extensive chromosomal variation, parapatric distribution patterns, and narrow hybrid zones at their boundaries. This species group stimulated development of one of the classic chromosomal speciation models, the stasipatric speciation model proposed by White in 1968. Our population genetic and phylogeographic analyses revealed extensive non-monophyly of chromosomal races along with historical and on-going gene introgression between them. These findings suggest that geographical isolation leading to the fixation of chromosomal variants in different geographic regions, followed by secondary contact, resulted in the present day parapatric distributions of chromosomal races. The significance of chromosomal rearrangements in the diversification of the viatica species group can be explored by comparing patterns of genetic differentiation between rearranged and co-linear parts of the genome.

No MeSH data available.