Hybridization: no longer the bad guy

It is interesting how some ideas get stuck in our minds even long after it is proved that they are incorrect or incomplete. Haeckel’s Recapitulation Theory, which states that during the embryological development of an organism it undergoes through different stages recalling the evolutionary history of its ancestors (ontogeny recapitulates phylogeny), is considered obsolete nowadays. However, it is not very difficult to find in textbooks the well-known and controversial drawings comparing different vertebrate embryos with an ambiguous caption that may lead to incorrect interpretations. Frequently, biology students will misunderstand why all these embryos are similar at the early stages, probably because the Recapitulation Theory is easy to assimilate and seems to “make sense” when read in a textbook. Apparently, it takes a long time to get rid of scientific ideas that are, at best, just partially right. Another example of a concept that is only incompletely understood by a majority of people interested in science is hybridization. Historically, hybridization has been linked to processes that make difficult the origin of new species (speciation) homogenizing the genetic diversity of different populations. This perception can be easily understood if we summarize how this event was first approached.

Hybridization has played a very important role in the way we conceive species and speciation since the beginnings of the modern evolutionary paradigm. In the Origin, Darwin devoted a whole chapter to this issue, mainly because it was one of his greatest worries: if the natural selection can stabilize new traits of a population, premature hybridization of this population with others may act as a “dissolving force” that countervails what natural selection achieved, thus preventing new species to be born. Ultimately, Darwin shared his perception of hybrids with animal and plant breeders, who during generations select the preferred traits to obtain the desired animals or plants; in this context, hybrids may indeed ruin the breeder’s work. After speciation has occurred, interspecific hybrids are thought to be sterile, and hybridization becomes a natural barrier that keeps the integrity of each species. Consequently, reproductive isolation can be used as criterion to test species delimitation. This idea was further developed a century later by Ernst Mayr under the term “biological species concept”, gaining considerable popularity.

Research on hybridization, both, below and over the species level, has been conducted regularly during the last decades. Interestingly, it does not seem that all the new knowledge has been widely assimilated, and many people still continue thinking like pigeon breeders and considering hybridization merely the “bad guy” of the speciation stories. This opinion would likely change if we keep in mind the advances in both, the co-called “species problem”, and the hybridization itself.

Firstly, the species conceptualization was subject of an intense discussion during most part of the 20^th century¹. The biological species concept was criticized by the advocates of the phylogenetic concepts because of its lack of universal applicability: it is useless within organisms without sexual reproduction and it neglects the existence of distinct, fertile hybrids that were already known to be widespread, for instance, in plants. Although the species problem is still a matter of debate, the early 21^st century brought some interesting ideas that point towards a common understanding of the different concepts². Moreover, the differences among these concepts may be interpreted as conflictive only in the “grey area” where the speciation process is taking place, but coincident elsewhere³. It is precisely in that area of uncertainty where hybridization may play an unpredictable an interesting role.

The latest issue of the Journal of Evolutionary Biology includes a review⁴ on the state of the art of the relation between hybridization and the occurrence of new species. It summarizes a discussion that took place in 2011 in the context of a monographic symposium in Wales, and it is a good read if we need some update on this topic. The main idea is that the current knowledge suggests that hybridization plays a significant role which is not limited to a homogenization of the diversity, but may indeed stimulate an active rapid genetic divergence and the formation of new, stable lineages.

The frequency of hybridization processes should be also reconsidered, since apparently they occur really often: about 10-30% of all multicellular organisms may hybridize regularly, and it is estimated that hybrid individuals are relatively frequent in sympatry⁵. Compared with the divergence caused by the cumulative mutations and later selection, the introgression of multiple alleles at the same time via hybridization is known to produce faster and more effective changes in the genome with immediate consequences that may include the induction of reproductive barriers and, hence, speciation⁶. According to the review, these mechanisms comprise (but may be not limited to): assortative mating and sexual selection, ecological divergence or Dobzhansky-Muller incompatibilities; all of them well documented in population biology.

Allopolyploids, stable polyploids with chromosomes from two or more different species, are also product of hybridization and a very well known speciation mechanism in plants. It is still surprising to realize that about 15% of all angiosperms and more than 30% of all the fern species were probably originated by allopolyploidy. Although not as frequent, hybridization and changes in the ploidy number has been also found in animals, and its importance has been probably underestimated in the past.

It seems that we have enough information to state that hybridization should not be considered only an obstacle for genetic divergence, but also a potential source of new species. However, the next challenges include the development of a methodology that makes possible to resolve if a particular taxon was originated by genome hybridization and, eventually, determine which the ancestors were. The modern high throughput sequencing techniques will probably make this possible. In fact, the ongoing genomic research of hybrids has already detected that the processes derived from hybridization at the molecular level may be much more complex than it was expected⁷ and that the contact of heterogeneous genomes itself may trigger further changes in the genomic architecture of the resulting hybrid⁸.

For how long will the hybridization keep only the “bad guy” role? Some textbooks should be immediately updated to stop reinforcing a long obsolete and partial idea. Interestingly, the importance of hybridization as a speciation enhancer is not new at all. Even at the same time as Mayr was advocating his biological concept, the botanist Edgar Anderson developed the idea of introgressive hybridization⁹; which is only gaining much recognition several decades after his death. It was once said by a colleague that “We used to make fun of Edgar Anderson by saying that he was finding hybrids under every bush. Then we realized that even the bushes were hybrids”[4].