insects

The Heliconius butterfly genome paper [1] is supercool for many reasons. Most important from my point of view is the attention to introgression among the different species of these South American butterflies.

The Heliconius reference genome allowed us to perform rigorous tests for introgression among melpomene–silvaniform clade species. We used RAD resequencing to reconstruct a robust phylogenetic tree based on 84 individuals of H. melpomene and its relatives, sampling on average 12 Mb, or 4%, of the genome (Fig. 1a and Supplementary Information, sections 12–18). We then tested for introgression between the sympatric co-mimetic postman butterfly races of Heliconius melpomene amaryllis and H. timareta ssp. nov. (Fig. 1) in Peru, using ‘ABBA/BABA’ single nucleotide sites and Patterson’s D-statistics (Fig. 3a), originally developed to test for admixture between Neanderthals and modern humans 21, 22 (Supplementary Information, section 12). Genome-wide, we found an excess of ABBA sites, giving a significantly positive Patterson’s D of 0.037 ± 0.003 (two-tailed Z-test for D = 0, P = 1 × 10−40), indicating greater genome-wide introgression between the sympatric mimetic taxa H. melpomene amaryllis and H. timareta ssp. nov. than between H. melpomene aglaope and H. timareta ssp. nov., which do not overlap spatially (Fig. 1b). On the basis of these D-statistics, we estimate that 2–5% of the genome was exchanged between H. timareta and H. melpomene amaryllis, to the exclusion of H. melpomene aglaope. (Supplementary Information, section 12). Exchange was not random. Of the 21 chromosomes, 11 have significantly positive D-statistics, and the strongest signals of introgression were found on the two chromosomes containing known mimicry loci B/D and N/Yb (Fig. 3b and Supplementary Information, section 15).

The paper goes on to demonstrate that color patterning genes have introgressed preferentially in cases where one geographically variable species mimics the local variants of another. Mimicry in these butterflies amounts to genetic theft, pure and simple.

I'll point out that the introgression of 2% of the genome is not a small amount. In the case of these butterflies, introgressed regions are clustered in particular areas, and some of them appear to have happened under the influence of selection (adaptive introgression). Still, there must be some strong reinforcement selection keeping the "species" reproductively separate enough to maintain their gene pools in the face of large-scale sympatric hybridization. Either that, or the current pattern is really a temporary snapshot of a longer, dynamic process of population dispersal and introgression.

There's also a section describing the extent of the chemosensory genes in butterflies, which have more than moths (34 compared to 23) despite their diurnality and greater reliance on visual cues. Funny to read of these being the most complicated insect olfaction systems yet known, considering the hundreds of olfactory receptors in mammalian genomes (UPDATE 2012-05-17: the paper refers to odorant-binding and chemosensory families, which are a subset of the total olfaction system [2]).

References

I can't believe the amount of attention the paper by Martin Nowak, Corina Tarnita and Edward O. Wilson [1] has gotten. It was in last week's Nature. The basic idea was that the evolution of eusociality in insects could be explained in a different way that the usual explanation, which involves calculating the relatedness of worker insects to their reproductive siblings. Eusociality has been one of the most visible applications of inclusive fitness theory -- that is, the observation that the fitness of a gene that alters behavior may be calculated in terms of its effects on the reproduction and survival of relatives. The paper notes that some aspects of eusociality are not well explained in terms of relatedness, and derives an alternative explanation.

The weird part of the paper is the way it describes inclusive fitness as some kind of theoretical afterthought, useful only as an ad hoc explanation for eusocial insects. It contrasts the inclusive fitness concept with "standard natural selection" as if it were possible for organisms to erase the fact that they're related to each other! And the authors imply that they have fatally damaged the concept of kin selection.

It's so contrary to evolutionary theory, that I thought maybe I was missing something. But I've been spending time on another problem this week and haven't had time to follow it up.

Fortunately, Jerry Coyne and Richard Dawkins have both given the paper some attention, and written notes and reactions to it. First Coyne ("A misguided attack on kin selection") reminds us of why kin selection has been such a successful part of "standard" evolutionary theory for the past fifty years.

Sex ratio theory, in which mothers produce different proportions of males and females, has been a particularly fruitful area for applying inclusive fitness theory. So has “altruism”—suicidal honeybees are just one example. And so are parental care and aspects thereof, especially parent-offspring conflict, a field brought to life by Bob Trivers using inclusive fitness theory. How else can you explain weaning conflict except by a conflict between the mother’s genetic welfare and that of her offspring?

I’m baffled not only by Nowak et al.’s apparent and willful ignorance of the literature, but by statements that are just wrong. They flatly assert, for instance, that “inclusive fitness theory” is something different from “standard natural selection theory.” But it’s not: it’s simply a natural extension of population genetics to the situation in which one’s behavior affects related individuals.

Richard Dawkins has also posted notes about the paper:

Kin selection is not a subset of group selection, it is a logical consequence of gene selection. And gene selection is (everything that Nowak et al ought to mean by) 'standard natural selection' theory: has been ever since the neo-Darwinian synthesis of the 1930s. Inclusive fitness theory is not some kind of supernumerary excrescence, to be 'resorted to' only if 'standard natural selection theory' is found wanting (Misunderstanding One). On the contrary, inclusive fitness theory is one way of expressing what was logically inherent in the synthesis ever since Fisher and Haldane, but had been largely overlooked because people (with the exception of those two geniuses) didn't think about collateral kin.

Yes, unless they're going to repeal the Price equation, they'll have to rely on relatedness to explain those phenotypes that never occur in reproductive individuals. As Dawkins puts it, "You have to talk about shared genes in individuals, with conditional phenotypic expression."

References