Hybrid vigor: The best of both parents, or a genomic clash?

During evolution, mutations produce new lineages that gradually diverge in sequence and regulatory properties. Related strains or species can hybridize to produce viable offspring. Hybrids often outperform their parents, producing more biomass or growing more rapidly. This superior performance, termed heterosis, contrasts the more expected clash between the genomes, and has puzzled geneticists and evolutionary biologists for many years. In this review, we describe two classes of models explaining heterosis: the prevailing view attributes heterosis to rapid repair or enhancement of growth promoting pathways. An alternative view attributes heterosis to the impairment of growth-limiting pathways. The two classes are not mutually exclusive and can result from similar types of genetic interactions. We discuss the possible implications of heterosis on tradeoffs in species evolution. Addresses 1 Department of Molecular Genetics, Weizmann Institute of Science, Rehovot 7610001, Israel 2 Department of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot 7610001, Israel Corresponding authors: Barkai, Naama (Naama.Barkai@weizmann. ac.il); Levy, Avraham A ([email protected]) Current Opinion in Systems Biology 2017, 6:22–27 This review comes from a themed issue on Systems biology of model organisms (2017) Edited by Jens Nielsen and Kiran Raosaheb Patil For a complete overview see the Issue and the Editorial Available online 24 August 2017 http://dx.doi.org/10.1016/j.coisb.2017.08.004 2452-3100/© 2017 Published by Elsevier Ltd. Introduction: hybrids and hybrid vigor Biological processes maintain a robust function in a wide range of environmental conditions and genetic polymorphism. Perhaps the most striking manifestations of this robustness are cases of inter-species hybridization, where mating of two distinct species generates viable offspring. Thus, despite large-scale differences in the genetic makeup and regulatory properties of the two parents, basic cellular and organismal properties are maintained upon mixing the two genomes. What is the mechanistic basis of hybrid robustness? How is it manifested at the molecular and cellular level? And how Current Opinion in Systems Biology 2017, 6:22–27 can the study of hybrids teach us about genome organization and evolution? Hybrids are produced upon mating parents from evolutionary related strains or species. Naively, one may expect that the hybrid will present an intermediate physiology, e.g. producing biomass similar to its parents’ median. In many cases, however, the hybrid physiology differs greatly from that of its parents [1e3]. New quantitative properties that emerge in hybrids are classified into two categories: properties that indicate hybrid incompatibility and properties that indicate hybrid vigor. Hybrid incompatibility refers to the expected cases in which the hybrid appears inferior to its parents, likely due to clashes between the two genomes. More surprising, perhaps, are cases of hybrid vigor, where the hybrid phenotype appears superior to that of its parents, producing, for example, more biomass, growing more rapidly, or showing increased stress survival [3e6]. Hybrid vigor, also termed heterosis, is ubiquitous in nature, and is observed in all eukaryotic kingdoms including plants, animals and fungi [2,4,7]. It has been exploited for thousands of years in plant and animal breeding in order to increase yield [3,8e11], and in fungi for improving alcoholic drinks, or, more recently, biofuel [4,12e14]. Perhaps the most profound example is maize crops, where hybrids have been used commercially in agriculture for nearly a century in order to increase yield, resulting in hybrid maize currently making up most of the corn yield worldwide [9,15]. Hybridization is also commonly used in order to increase yield in other crops such as rice, sorghum, and sunflower [9]. Heterosis has fascinated scientists since the early days of Darwin [1] and had been extensively researched ever since. Still, its mechanistic basis remains elusive [2]. How could the mixing of two distinct genomes, both of which underwent evolutionary optimization, result in an apparent superior performance? What makes heterosis ubiquitous and what does it tell us about possible constraints and limitations of species evolution? In this review, we discuss two classes of mechanisms that can explain heterosis (Figure 1). First, the prevailing model attributes hybrid vigor to an effective repair, or enhancement of growth promoting pathways. Such enhancement can be due to compensation of deleterious mutations through heterozygote www.sciencedirect.com