A Boolean gene regulatory model of heterosis and speciation
BMC Evol Biol, 15 (1):
24 (2015)DOI: 10.1186/s12862-015-0298-0
Abstract
Background: Modelling genetic phenomena affecting biological traits is important for the development of
agriculture as it allows breeders to predict the potential of breeding for certain traits. One such phenomenon is
heterosis or hybrid vigor: crossing individuals from genetically distinct populations often results in improvements in
quantitative traits, such as growth rate, biomass production and stress resistance. Heterosis has become a very
useful tool in global agriculture, but its genetic basis remains controversial and its effects hard to predict. We have
taken a computational approach to studying heterosis, developing a simulation of evolution, independent
reassortment of alleles and hybridization of Gene Regulatory Networks (GRNs) in a Boolean framework. These
artificial regulatory networks exhibit topological properties that reflect those observed in biology, and fitness is
measured as the ability of a network to respond to external inputs in a pre-defined way.
Results: Our model reproduced common experimental observations on heterosis using only biologically justified
parameters, such as mutation rates. Hybrid vigor was observed and its extent was seen to increase as parental
populations diverged, up until a point of sudden collapse of hybrid fitness. Thus, the model also describes a process
akin to speciation due to genetic incompatibility of the separated populations. We also reproduce, for the first time in a
model, the fact that hybrid vigor cannot easily be fixed by within a breeding line, currently an important limitation of
the use of hybrid crops. The simulation allowed us to study the effects of three standard models for the genetic basis
of heterosis: dominance, over-dominance, and epistasis.
Conclusion: This study describes the most detailed simulation of heterosis using gene regulatory networks to date and
reproduces several phenomena associated with heterosis for the first time in a model. The level of detail in our model
allows us to suggest possible warning signs of the impending collapse of hybrid vigor in breeding. In addition, the
simulation provides a framework that can be extended to study other aspects of heterosis and alternative evolutionary
scenarios.
Keywords: Heterosis, Gene regulatory network, Boolean network, Simulation, Speciation, Dominance, Overdominance,
Epistasis