The role of chromosome rearrangements
in reproductive isolation and speciation
(chromosomal speciation, particularly in plants)
Coghlan et al. (2005)
Are chromosomal rearrangements merely a problem for the genome, or do they
have functional significance in the short term (e.g. by enabling a species to
adapt to changing environmental conditions) or in the long term (e.g. by
facilitating speciation)?
Problems
Both morphologically distinct species that lack chromosomal differences (e.g. translocations and
inversions) and morphologically cryptic species with chromosomal differences can be found
The amount of phenotypic evolution is not a good predictor of the
amount of karyotypic evolution
Are chromosome rearrangements important for
creating reproductive isolation barriers and speciation?
Or is the accumulation of chromosomal differences
between populations largely incidental to speciation?
(e.g., = speciation  chromosome rearrangements)
M.J.D. White
YES!
Cryptic species with population-specific
chromosome rearrangements?
Grund et al. 2006, PNAS 103
Draba nivalis
See also:
Gustafsson ALS, Skrede I, Rowe HC, Gussarova G, Borgen L, et al. (2014) Genetics of Cryptic Speciation
within an Arctic Mustard, Draba nivalis. PLoS ONE 9(4): e93834. doi:10.1371/journal.pone.0093834
Grund et al. 2006, PNAS 103:
Although 99% of parental individuals were fully fertile, the
fertility of intraspecific crosses was surprisingly low. Hybrids
from crosses within populations were mostly fertile (63%), but
only 8% of the hybrids from crosses within and among
geographic regions (Alaska, Greenland, Svalbard, and Norway)
were fertile.
The frequent occurrence of intraspecific crossing barriers is not
accompanied by significant morphological or ecological
differentiation, indicating that numerous cryptic biological
species have arisen within each taxonomic species despite their
recent (Pleistocene) origin.
Draba nivalis
Cryptic species with population-specific
chromosome rearrangements?
Models of chromosomal speciation (Rieseberg 2001)
• Chain or Cascade models
• Chromosomal transilience model
• Monobrachial fusion model
• Recombinational model
• Quantum speciation model
• Stasipatric model
• Saltational model
References
White, M.J.D. (1978) Modes of Speciation.
Templeton, A.R. (1981) Mechanisms of speciation – a population
genetic approach. Annu. Rev. Ecol. Syst. 12, 23–48.
Baker, R.J. and Bickham J.W. (1986) Speciation by monobrachial
centric fusions. Proc. Natl. Acad. Sci. U. S. A. 83, 8245–8248.
Grant, V. (1981) Plant Speciation.
Lewis, H. (1966) Speciation in flowering plants. Science 152, 167–
172.
Fundamental feature of the models: chromosomal differences that have
accumulated between the neospecies and its progenitor(s) are assumed
to impair the fertility or viability of interspecific hybrids, thereby reducing
gene flow
Deviating features of the models:
• geographical isolation is (not) required for speciation
• the means by which chromosomal rearrangements arise and become fixed
• effects of rearrangements on the fitness of chromosomally heterozygous individuals
Chromosomal speciation: problems
• newly arisen chromosomal rearrangements
will exist in the population almost exclusively as
heterozygotes (inversion or translocation
heterozygotes)
• many chromosomal rearrangements have little effect on fertility
(ineffectiveness of chromosomal differences as barriers to gene flow)
• novel chromosomal arrangements have a selective disadvantage when they
first appear in a population:
the problem of underdominance: difficulties associated with fixing chromosomal
rearrangements that are strongly underdominant (i.e. reduce the fitness of
heterozygotes)
Two models:
o the hybrid-sterility model
o recombination-suppression model
Chromosomal speciation
Suppressed-recombination model (Rieseberg 2001, Noor et al. 2001)
Experimental data
Drosophila
- inversions have contributed to speciation between the close relatives D. pseudoobscura and
D. persimilis: inversions are found within the genomic regions associated with hybrid sterility
- chromosomal rearrangements reduce recombination between the genomes of the species,
thereby enabling genetic differences to accumulate within the rearranged regions
- inversions are more common between Drosophila species that are sympatric compared to
allopatric pairs (also true for butterflies)
Plants
- the exact relationship between chromosomal rearrangement and speciation remains unclear
in plants! ....but it is expected and probable
- sunflowers (Helianthus), Mimulus
Chromosome rearrangements provide large regions of the
genome protected from gene flow where isolating genes
may accumulate until complete reproductive barriers
exist.
Suppressed-recombination model
(Rieseberg 2001, Noor et al. 2001, Faria and Navarro 2010)
The model suggests that rearrangements may reduce gene
flow by suppressing recombination. CRs allow genes located
in these regions to differentiate, in contrast to genes in
freely recombining collinear regions.
A paracentric inversion in D. pseudoobscura
• gross chromosomal rearrangements in Drosophila are well characterized as
rearrangements are easily detected in the chromosomes of their giant salivary glands
• the most common type of gross chromosomal rearrangement are paracentric inversions
(do not span the centromere)
• paracentric inversions are common polymorphisms in drosophilas and other fly species
(different populations of D. melanogaster harbor more than 500 inversion polymorphisms)
Chromosome speciation in Drosophila
Inversions are crossover suppresors –
evolutionary consequences (speciation)
Anopheles gambiae
(a) Polymorphic paracentric inversions in A.
gambiae chromosome arm 2R.
(b) Three non-interbreeding populations of A.
gambiae (named Bamako, Savanna and Mopti) that
live in the same region of Mali. The 3 populations
differ by chromosomal inversions that might be
contributing to speciation in A. gambiae. (For
example, a chromosome with arrangement 2R jcu has
inversions j, c and u on chrosmosome arm 2R.)
Do chromosomal rearrangements contribute to
speciation in Anopheles gambiae?
The role of chromosomal rearrangements in speciation in the A. gambiae species
complex is difficult to prove: even a highly significant coincidence in time between
chromosomal rearrangements and speciation does not prove a causal relationship.
Love et al. (2016), Mol Ecol
• initial genomic and ecological differentiation
– sympatric speciation
• the majority of differentiated regions
between Bamako and typical An. gambiae
are located inside inversions
• differentiated genomic regions were
enriched for genes implicated in nervous
system development and signalling
Bamako
Suppressed-recombination model
PLANTS
• the exact relationship between chromosomal rearrangement and speciation remains
unclear in plants! ...but more evidence is emerging (new methods available)
• seems that sunflowers (Helianthus) are only example: hybridization between two
divergent diploid species appears to have provoked speciation events in sunflowers (Loren
Rieseberg’s lab) ....and recently Mimulus guttatus (Lowry and Willis 2010)
Hybrid
Homoploid
Chromosomal
Recombinational
speciation in sunflowers (Helianthus)
The rate of introgression is lower within rearranged chromosomes
/chromosome regions (vs. collinear regions). The strongest difference close to
the breakpoints - consistent with suppressed-recombination models (the
strongest reduction in recombination).
Hybrid
Homoploid
Chromosomal
Recombinational
 three Helianthus species are probably the best documented examples of homoploid hybrid
speciation in either animals or plants
 hybrid or recombinational speciation refers to the origin of a new homoploid species
via hybridization between chromosomally or genetically divergent parental species
 homoploid hybrid speciation is theoretically difficult because it requires the development
of reproductive barriers in sympatry or parapatry (the possibility of backcrossing with their
parental species)
 theory suggests that isolation may arise through rapid karyotypic evolution and/or
ecological and spatial divergence of hybrid neospecies
speciation in sunflowers (Helianthus)
 it is assumed that new hybrid lineage diverge karyotypically from its parental species
through the chromosomal rearrangements that differentiate the parental species and/or by
new chromosomal rearrangements induced by recombination
Helianthus annuus Helianthus petiolaris
Helianthus anomalus
• a sand dune endemic, central Utah and northern Arizona
• both parental species are widespread; hybridize but retain their
genetic integrity because of the synergistic action of several
reproductive barriers
• three experimentally generated hybrid lineages (H. annuus x H.
petiolaris) showed a combination of chromosomal blocks similar to that
found in H. anomalus (Rieseberg et al. 1996)
• the three synthetic lineages were cross-compatible with each other
and with H. anomalus (Rieseberg 2000)
• H. anomalus has diverged considerably from its
parents in both karyotype and ecological preference
due to the sorting of chromosomal rearrangements
that differentiate the parental species. H. anomalus
also possesses several unique arrangements,
possibly induced by recombination. As a result, H.
anomalus is almost completely intersterile with its
parental species
Homoploid hybrid speciation: H. anomalus
H. annuus x H. petiolaris
H. anomalus
Homoploid hybrid speciation in sunflowers (Helianthus)
• the remainder of karyotypic differences appear to
have arisen de novo (6 breakages/6 fusions in H.
anomalus, 4 breakages/3 fusions in H. deserticola, and
5 breakages/5 fusions in H. paradoxus)
 it is assumed that new hybrid lineage diverge karyotypically from its parental species through the
chromosomal rearrangements that differentiate the parental species and/or by new chromosomal
rearrangements induced by recombination
H. annuus x H. petiolaris
H. anomalus
H. deserticola
H. paradoxus
• karyotypes of the three hybrid species are massively
divergent from their parental species
• about one-third of the karyoypic differences
arose through the sorting of parental chromosomal
rearrangements
• karyotypic differences contribute to reproductive
isolation: 9 of 11 pollen viability QTLs occur on rearranged
chromosomes and all but one map close to a rearrangement
breakpoint
perennial and annual plant
yellow monkeyflower (Mimulus guttatus)
M. guttatus: geographic distribution of the chromosomal inversion
(A) Map of western North America with the locations of populations of coastal perennials (blue), inland annuals (orange),
and inland perennials (purple), as well as obligate self-fertilizing species M. nasutus (yellow). (B) Marker order of the AN
and PE inversion arrangements along linkage group eight. Inland annuals and M. nasutus had the AN arrangement while
coastal and inland perennials all had the PE arrangement.
o a geographically widespread adaptive inversion polymorphism in the yellow
monkeyflower (Mimulus guttatus)
o the inversion is involved in a classic life-history shift in plants - an adaptive response
to differences in the seasonal availability of water resources:
- one arrangement of the inverted region is found in an annual ecotype that lives in
Mediterranean habitats characterized by reduced soil water availability in the summer;
- the other arrangement appears in a perennial ecotype that lives in habitats with high yearround
soil moisture.
o inversion polymorphism influences morphological and flowering time differences
between the two ecotypes = reproductive isolating barriers
o observation is consistent with the theory that adaptation to local environments can
drive the spread of chromosomal inversions and promote speciation.
o for the first time in nature was shown the contribution of an inversion to adaptation,
an annual/perennial life-history shift, and multiple reproductive isolating barriers
Inversion polymorphism and adaptation in Mimulus
Chromosome „fusions“ (CF) as a speciation agent ?
Loci A and B segregate
independently in unfused
homozygotes, recombination has
different rates and segregation is
different in heterozygotes and
fused homozygotes
o CF can lead to tight linkage of genes („super-gene“)
o ... can avoid recombination between locally adapted alleles –
adaptation / divergence / speciation
o ... can alter gene expression (silencing or higher expression)
o ...can confer mechanistic advantage (decreased no. of
chromosomes = faster processes = possible adaptive
advantage)
Chromosome „fusion“ – the origin of the human (dicentric) chromosome 2
2n = 48
2n = 46
Chromosome „fusion“ – the origin of the human (dicentric) chromosome 2
inactive centromere
active centromere
Chiatante et al. (2017), MBE
Chromosome „fusion“ – the origin of the human (dicentric) chromosome 2
Chiatante et al. (2017), MBE
Two optionss how the „fusion“ chromosome 2 was stabilized
• the ancestral centromere (AC) was either epigenetically inactivated or centromeredetermining
sequences were excised
• the excision is more probable – what mechanism?
• recombination-based excision, most likely in one step (similar human clinical cases...)
Did the origin of „fusion“ chromosome 2 contributed to reproductive
isolation of hominid species from great apes?
2n = 48
2n = 46
• different no. of chromosomes  reproductive isolation
• loss of gene(s)  adaptive advantage
• gene linkage? changed regulation of gene expression?
Potter et al. (2017), Front Genet
Chromosomal speciation – example of rock-wallabies
Potter et al. (2017), Front Genet
Chromosomal speciation – example of rock-wallabies
• chromosome „fusions“ via
reciprocal translocations
• inversions
• centromere shifts
Speciation by Robertsonia translocations („centric fusions“)
Ahola et al., Nat Comm (2014)
The Glanville fritillary genome retains an ancient karyotype and
reveals selective chromosomal „fusions“ in Lepidoptera
• Lepidoptera: n = 5 to 223
• the ancestral
lepidopteran karyotype
has been n = 31 for at
least 140 million years
• karyotype evolution
through chromosome
„fusions“