Abstract
When hybrid inviability is an indirect by-product of local adaptation, we expect its degree of severity between pairs of populations to vary and to be sensitive to the environment. While complete reciprocal hybrid inviability is the outcome of the gradual process of local adaptation, it is not representative of the process of accumulation of incompatibility. In the flour beetle, Tribolium castaneum, some pairs of populations exhibit complete, reciprocal F1 hybrid incompatibility while other pairs are fully or partially compatible. We characterize this naturally occurring variation in the degree and timing of expression of the hybrid incompatible phenotype to better understand the number of genes or developmental processes contributing to speciation. We assessed the morphological and developmental variation in four Tribolium castaneum populations and their 12 possible F1 hybrids at each life-history stage from egg to adult. We find that the rate of hybrid larval development is affected in all interpopulation crosses, including those eventually producing viable, fertile adults. Hybrid incompatibility manifests early in development as changes in the duration of instars and diminished success in the transition between instars are relative to the parent populations. Parent populations with similar developmental profiles may produce hybrids with disrupted development. The degree and timing of expression of hybrid inviability depends upon populations crossed, direction of the cross, and environment in which hybrids are raised. Our findings suggest that the coordinated expression of genes involved in transitional periods of development is the underlying cause of hybrid incompatibility in this species.
Highlights
Previous work by Demuth and Wade (2007a,b) discovered widespread adult hybrid incompatibility among populations of the red flour beetle, T. castaneum: 3% to 100% of adult interpopulation hybrids exhibit negative phenotypes such as deformities of the limbs, antennae, mouthparts, and wings
The variation observed within the T. castaneum species for interpopulation compatibility represents the “polymorphic prelude to BDM incompatibilities” (Cutter 2012), affording an opportunity to dissect the genetic causes of incompatibility early in the speciation process
We find that hybrid incompatibility manifests early in development as changes in the duration of larval instars and as diminished success in the transition between instars relative to the pure-bred parent populations
Summary
Previous work by Demuth and Wade (2007a,b) discovered widespread adult hybrid incompatibility among populations of the red flour beetle, T. castaneum: 3% to 100% of adult interpopulation hybrids exhibit negative phenotypes such as deformities of the limbs, antennae, mouthparts, and wings. Some interpopulation crosses exhibited Haldane’s Rule (Demuth and Wade 2007b), wherein the heterogametic male hybrids exhibited more frequent deformities than their homogametic hybrid sisters. The variation observed within the T. castaneum species for interpopulation compatibility represents the “polymorphic prelude to BDM incompatibilities” (Cutter 2012), affording an opportunity to dissect the genetic causes of incompatibility early in the speciation process. These data support the view that hybrid incompatibility is an indirect by-product of adaptation to local environments, with some population pairs more divergent, and more incompatible, than others
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