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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.


(a) Parapatric distribution of chromosomal races of the viatica species group in southeastern Australia proposed by White et al. [21,23]. An inset shows distribution of three races on Kangaroo Island. A 100 m isobath is indicated as a proxy of an ancient coastline at glacial maxima during the Pleistocene. Karyotypes of each race (♂)/(♀) are: viatica19, 2n = 19/20, XO/XX; viatica17, 2n = 17/18, XO/XX; P24(XO), 2n = 17/18, XO/XX; P24(XY), 2n = 16, XY/XX; P24(XY)-Translocation, 2n = 16, XY/XX; P25(XO), 2n = 19/20, XO/XX; P25(XY), 2n = 18, XY/XX; P45b(XO), 2n = 19/20, XO/XX; P45b(XY), 2n = 18, XY/XX; P50, 2n = 19/20, XO/XX; V. pichirichi, 2n = 19/20, XO/XX. (b) Thirteen genetic clusters resolved by the Bayesian clustering analysis using 35 allozyme loci, superimposed on a distribution map. Red circles with solid line indicate clusters shared among multiple chromosomal races. Four taxa [P24(XY), P24(XY)-Translocation, P45c, and V. pichirichi] comprise exclusive genetic clusters (blue circles with dashed line).
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f1-insects-02-00049: (a) Parapatric distribution of chromosomal races of the viatica species group in southeastern Australia proposed by White et al. [21,23]. An inset shows distribution of three races on Kangaroo Island. A 100 m isobath is indicated as a proxy of an ancient coastline at glacial maxima during the Pleistocene. Karyotypes of each race (♂)/(♀) are: viatica19, 2n = 19/20, XO/XX; viatica17, 2n = 17/18, XO/XX; P24(XO), 2n = 17/18, XO/XX; P24(XY), 2n = 16, XY/XX; P24(XY)-Translocation, 2n = 16, XY/XX; P25(XO), 2n = 19/20, XO/XX; P25(XY), 2n = 18, XY/XX; P45b(XO), 2n = 19/20, XO/XX; P45b(XY), 2n = 18, XY/XX; P50, 2n = 19/20, XO/XX; V. pichirichi, 2n = 19/20, XO/XX. (b) Thirteen genetic clusters resolved by the Bayesian clustering analysis using 35 allozyme loci, superimposed on a distribution map. Red circles with solid line indicate clusters shared among multiple chromosomal races. Four taxa [P24(XY), P24(XY)-Translocation, P45c, and V. pichirichi] comprise exclusive genetic clusters (blue circles with dashed line).

Mentions: Australian morabine grasshoppers of the genus Vandiemenella (the viatica species group) provide an excellent study system to investigate potential roles of chromosomal rearrangements in speciation because they show extensive chromosomal variation, with 12 known chromosomal races/species [2,21]. These taxa have been discriminated by chromosomal rearrangements (fusions, fissions, translocations, or inversions), characters of the external genitalia, and morphometrics [21,22]. With only two exceptions, most taxa have parapatric distributions, in a mosaic pattern within South Australia (SA), and often form narrow contact zones at their boundaries (Figure 1a). White and colleagues carried out extensive studies of a number of the hybrid zones on Kangaroo Island and the mainland of SA, and controlled breeding studies of hybrids between a number of the chromosomal races, providing a background of data on the chromosomal variation and fitness of hybrids [21–27]. In contact zones, two different chromosomal taxa meet, hybridize, and produce at least some offspring of mixed ancestry, forming a smooth transition of chromosomal, morphological, and some heritable characters (each character transition is termed a ‘cline’). Largely based on these studies in the viatica species group, White argued that chromosomal changes play a causative role in speciation by leading to hybrid dysfunction or underdominance of heterokaryotypic individuals and proposed a classic chromosomal speciation model, called the ‘stasipatric speciation model’ [2,28]. Key features of this model include (i) chromosomal rearrangements produce barriers to gene flow between parental and daughter chromosome types due to meiotic abnormalities in chromosomal heterozygotes, and (ii) the spread of new chromosome types from their point of origin into the distribution of a parental chromosome type occurs without geographic isolation, leading to parapatric distributions of chromosomal races. However, because this model also suffers from the theoretical problems described earlier, this mechanism is no longer considered viable [1].


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

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

(a) Parapatric distribution of chromosomal races of the viatica species group in southeastern Australia proposed by White et al. [21,23]. An inset shows distribution of three races on Kangaroo Island. A 100 m isobath is indicated as a proxy of an ancient coastline at glacial maxima during the Pleistocene. Karyotypes of each race (♂)/(♀) are: viatica19, 2n = 19/20, XO/XX; viatica17, 2n = 17/18, XO/XX; P24(XO), 2n = 17/18, XO/XX; P24(XY), 2n = 16, XY/XX; P24(XY)-Translocation, 2n = 16, XY/XX; P25(XO), 2n = 19/20, XO/XX; P25(XY), 2n = 18, XY/XX; P45b(XO), 2n = 19/20, XO/XX; P45b(XY), 2n = 18, XY/XX; P50, 2n = 19/20, XO/XX; V. pichirichi, 2n = 19/20, XO/XX. (b) Thirteen genetic clusters resolved by the Bayesian clustering analysis using 35 allozyme loci, superimposed on a distribution map. Red circles with solid line indicate clusters shared among multiple chromosomal races. Four taxa [P24(XY), P24(XY)-Translocation, P45c, and V. pichirichi] comprise exclusive genetic clusters (blue circles with dashed line).
© Copyright Policy
Related In: Results  -  Collection

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

f1-insects-02-00049: (a) Parapatric distribution of chromosomal races of the viatica species group in southeastern Australia proposed by White et al. [21,23]. An inset shows distribution of three races on Kangaroo Island. A 100 m isobath is indicated as a proxy of an ancient coastline at glacial maxima during the Pleistocene. Karyotypes of each race (♂)/(♀) are: viatica19, 2n = 19/20, XO/XX; viatica17, 2n = 17/18, XO/XX; P24(XO), 2n = 17/18, XO/XX; P24(XY), 2n = 16, XY/XX; P24(XY)-Translocation, 2n = 16, XY/XX; P25(XO), 2n = 19/20, XO/XX; P25(XY), 2n = 18, XY/XX; P45b(XO), 2n = 19/20, XO/XX; P45b(XY), 2n = 18, XY/XX; P50, 2n = 19/20, XO/XX; V. pichirichi, 2n = 19/20, XO/XX. (b) Thirteen genetic clusters resolved by the Bayesian clustering analysis using 35 allozyme loci, superimposed on a distribution map. Red circles with solid line indicate clusters shared among multiple chromosomal races. Four taxa [P24(XY), P24(XY)-Translocation, P45c, and V. pichirichi] comprise exclusive genetic clusters (blue circles with dashed line).
Mentions: Australian morabine grasshoppers of the genus Vandiemenella (the viatica species group) provide an excellent study system to investigate potential roles of chromosomal rearrangements in speciation because they show extensive chromosomal variation, with 12 known chromosomal races/species [2,21]. These taxa have been discriminated by chromosomal rearrangements (fusions, fissions, translocations, or inversions), characters of the external genitalia, and morphometrics [21,22]. With only two exceptions, most taxa have parapatric distributions, in a mosaic pattern within South Australia (SA), and often form narrow contact zones at their boundaries (Figure 1a). White and colleagues carried out extensive studies of a number of the hybrid zones on Kangaroo Island and the mainland of SA, and controlled breeding studies of hybrids between a number of the chromosomal races, providing a background of data on the chromosomal variation and fitness of hybrids [21–27]. In contact zones, two different chromosomal taxa meet, hybridize, and produce at least some offspring of mixed ancestry, forming a smooth transition of chromosomal, morphological, and some heritable characters (each character transition is termed a ‘cline’). Largely based on these studies in the viatica species group, White argued that chromosomal changes play a causative role in speciation by leading to hybrid dysfunction or underdominance of heterokaryotypic individuals and proposed a classic chromosomal speciation model, called the ‘stasipatric speciation model’ [2,28]. Key features of this model include (i) chromosomal rearrangements produce barriers to gene flow between parental and daughter chromosome types due to meiotic abnormalities in chromosomal heterozygotes, and (ii) the spread of new chromosome types from their point of origin into the distribution of a parental chromosome type occurs without geographic isolation, leading to parapatric distributions of chromosomal races. However, because this model also suffers from the theoretical problems described earlier, this mechanism is no longer considered viable [1].

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.