Speciation: a Few Big Genes or Many Little Ones?
by Simon Martin, Richard Merrill and Chris Jiggins
NOTE: This blog post has been substantially abridged and edited by PLOS Biologue. For the full-length text, please see Heliconius.org.
This month, we published two papers in PLOS Biology on the genetic architecture of speciation in Heliconius butterflies, among the best-known study systems in speciation research. Both papers represent the culmination of many years of work, but at first glance appear to come to contradictory conclusions. In this piece we discuss why this is the case, and show how it relates to a broader debate about the importance of major loci versus polygenic effects in evolution.
In fact, from the start our two papers approach the same system from different directions. In the first paper, by Merrill et al., we focus on the fact that two closely-related species that co-occur in Panama (Heliconius melpomene and H. cydno) have evolved strong assortative mating behaviour: they really do not like to hybridize, and much prefer to mate with their own kind. This paper asked about the gene(s) underlying divergence in these preference behaviours, which would inform us about a key step in the evolution of distinct species from a common ancestor.
In contrast, in the second paper, by Martin et al., we start from the knowledge that these two species are in fact capable of producing fertile male hybrids, and that their genomes carry the signatures of extensive genetic mixing, or ‘admixture.’ While hybridisation is rare (on a per-individual basis) very occasional inter-species mating is enough to scramble the genomes of two species if it occurs over millions of generations. This second paper therefore addresses how natural selection is acting against the hybrids and their offspring (which will carry a combination of genes from both species) to keep the species distinct despite their potential to become genetically mixed.
The main finding of the Merrill et al. paper is that just three genetic loci control a large proportion of differences in mating preference between the species. Remarkably, one of these loci controls both the colour of the butterfly wings and preference for that colour (though this does not necessarily imply that the same genes are involved). The discovery that changes in a complex behaviour can arise through changes at just a few loci seems surprising, and has important implications for speciation. A new species can arise much more readily if natural selection can act on a few genes of large effect, rather than many loci of small effect. This genetic system that we have discovered should therefore make speciation easier.
By contrast, Martin et al. show that the landscape of admixture between these species is consistent with a highly ‘polygenic’ barrier, in which the species boundary is maintained by natural selection acting at multitudes of ‘barrier loci’ across the genome, suggesting a minor contribution of any given locus. This joins a number of studies showing similar trends in both plants and animals. So how do we reconcile these findings? Is speciation more dependent on a few major-effect loci that prevent hybridisation, or many small-effect loci that lead to the elimination of hybrids?
We think there is less of a paradox here than first appears, and that the papers are more complementary than contradictory. This is because the papers not only consider different components of speciation (pre-mating versus post-mating isolation), but also use different strategies (trait-focused versus genome-focused approaches).
Most speciation events probably involve both pre-mating and post-mating isolating mechanisms: those that limit the production of hybrids as well as those that reduce the survival and reproductive output of any hybrids that are produced. It is perhaps unsurprising that by dissecting these different levels at which isolating mechanisms act, we find different genetic architectures. The two studies also used entirely different methodologies, designed to detect different things. The approach of Merrill et al., called QTL mapping, is classed as ‘forward genetics’, which starts with a trait of interest and identifies the loci that are associated with that trait; Martin et al., by contrast, used a ‘reverse-genetics’ approach, which starts by identifying signatures of selection in the genome, naive to the trait that is being selected.
In summary, we have found evidence both for a highly polygenic architecture, but also loci with major effects on species boundaries. An appealing story would be that early stages of speciation are characterised by ecological selection acting on a few loci of major effect, but that later stages involve accumulation of differences at many traits that are more polygenic – however we cannot distinguish the time-course of speciation from studies like these that represent a snapshot of a single species pair. There are also implications here for future speciation studies. The genome scan approach will not necessarily find loci with a large effect on species barriers, even where they exist. Even if no major ‘islands’ of reduced admixture are found, this does not preclude large-effect loci influencing specific traits. As is so often the case in biology, the reality does not fit any single narrative.
The Featured Image shows Heliconius cydno (left) and Heliconius melpomene (right) reluctantly mating in captivity. Credit: Chris Jiggins