Mimicry Genes Research Articles

Mimicry genes reduce pre-adult survival rate in Papilio polytes: A possible new mechanism for maintaining female-limited polymorphism in Batesian mimicry.

Batesian mimicry, in which harmless organisms resemble unpalatable or harmful species, is a well-studied adaptation for predation avoidance. The females of some Batesian mimic species comprise mimetic and nonmimetic individuals. Mimetic females of such polymorphic species clearly have a selective advantage due to decreased predation pressure, but the selective forces that maintain nonmimetic females in a population remain unclear. In the swallowtail butterfly, Papilio polytes, female polymorphism is controlled by the H (mimetic) and h (nonmimetic) alleles at a single autosomal locus. Here, we examined whether the dominant H allele has a deleterious effect on the pre-adult survival rate (egg-to-adult emergence rate). We repeated an assortative mating-like treatment-that is breeding of males and females whose mothers had the same phenotype (mimetic or nonmimetic)-for three consecutive generations, while avoiding inbreeding. Results showed that pre-adult survival rate decreased over generations only in lines derived from mothers with the mimetic phenotype (hereafter, mimetic-assorted lines). This lowered survival was due to an increased mortality at the final instar larval stage and the pupal stages. Interestingly, the pre-adult mortality in the mimetic-assorted lines seemed to be associated with a male-biased sex ratio at adult emergence. These results suggest that the dominant H allele displays a mildly deleterious effect that is expressed more strongly in females and homozygous individuals than in heterozygous individuals. We propose that this cost of mimicry in larval and pupal stages contributes to the maintenance of female-limited polymorphism in P.polytes.

Do Heliconius butterfly species exchange mimicry alleles?

Hybridization has the potential to transfer beneficial alleles across species boundaries, and there are a growing number of examples in which this has apparently occurred. Recent studies suggest that Heliconius butterflies have transferred wing pattern mimicry alleles between species via hybridization, but ancestral polymorphism could also produce a signature of shared ancestry around mimicry genes. To distinguish between these alternative hypotheses, we measured DNA sequence divergence around putatively introgressed mimicry loci and compared this with the rest of the genome. Our results reveal that putatively introgressed regions show strongly reduced sequence divergence between co-mimetic species, suggesting that their divergence times are younger than the rest of the genome. This is consistent with introgression and not ancestral variation. We further show that this signature of introgression occurs at sites throughout the genome, not just around mimicry genes.

Adaptive introgression in animals: examples and comparison to new mutation and standing variation as sources of adaptive variation

Adaptive genetic variation has been thought to originate primarily from either new mutation or standing variation. Another potential source of adaptive variation is adaptive variants from other (donor) species that are introgressed into the (recipient) species, termed adaptive introgression. Here, the various attributes of these three potential sources of adaptive variation are compared. For example, the rate of adaptive change is generally thought to be faster from standing variation, slower from mutation and potentially intermediate from adaptive introgression. Additionally, the higher initial frequency of adaptive variation from standing variation and lower initial frequency from mutation might result in a higher probability of fixation of the adaptive variants for standing variation. Adaptive variation from introgression might have higher initial frequency than new adaptive mutations but lower than that from standing variation, again making the impact of adaptive introgression variation potentially intermediate. Adaptive introgressive variants might have multiple changes within a gene and affect multiple loci, an advantage also potentially found for adaptive standing variation but not for new adaptive mutants. The processes that might produce a common variant in two taxa, convergence, trans-species polymorphism from incomplete lineage sorting or from balancing selection and adaptive introgression, are also compared. Finally, potential examples of adaptive introgression in animals, including balancing selection for multiple alleles for major histocompatibility complex (MHC), S and csd genes, pesticide resistance in mice, black colour in wolves and white colour in coyotes, Neanderthal or Denisovan ancestry in humans, mimicry genes in Heliconius butterflies, beak traits in Darwin's finches, yellow skin in chickens and non-native ancestry in an endangered native salamander, are examined.

Mimetic Butterflies Introgress to Impress

Mimetic Butterflies Introgress to Impress

Highly conserved gene order and numerous novel repetitive elements in genomic regions linked to wing pattern variation in Heliconius butterflies

BackgroundWith over 20 parapatric races differing in their warningly colored wing patterns, the butterfly Heliconius erato provides a fascinating example of an adaptive radiation. Together with matching races of its co-mimic Heliconius melpomene, H. erato also represents a textbook case of Müllerian mimicry, a phenomenon where common warning signals are shared amongst noxious organisms. It is of great interest to identify the specific genes that control the mimetic wing patterns of H. erato and H. melpomene. To this end we have undertaken comparative mapping and targeted genomic sequencing in both species. This paper reports on a comparative analysis of genomic sequences linked to color pattern mimicry genes in Heliconius.ResultsScoring AFLP polymorphisms in H. erato broods allowed us to survey loci at approximately 362 kb intervals across the genome. With this strategy we were able to identify markers tightly linked to two color pattern genes: D and Cr, which were then used to screen H. erato BAC libraries in order to identify clones for sequencing. Gene density across 600 kb of BAC sequences appeared relatively low, although the number of predicted open reading frames was typical for an insect. We focused analyses on the D- and Cr-linked H. erato BAC sequences and on the Yb-linked H. melpomene BAC sequence. A comparative analysis between homologous regions of H. erato (Cr-linked BAC) and H. melpomene (Yb-linked BAC) revealed high levels of sequence conservation and microsynteny between the two species. We found that repeated elements constitute 26% and 20% of BAC sequences from H. erato and H. melpomene respectively. The majority of these repetitive sequences appear to be novel, as they showed no significant similarity to any other available insect sequences. We also observed signs of fine scale conservation of gene order between Heliconius and the moth Bombyx mori, suggesting that lepidopteran genome architecture may be conserved over very long evolutionary time scales.ConclusionHere we have demonstrated the tractability of progressing from a genetic linkage map to genomic sequence data in Heliconius butterflies. We have also shown that fine-scale gene order is highly conserved between distantly related Heliconius species, and also between Heliconius and B. mori. Together, these findings suggest that genome structure in macrolepidoptera might be very conserved, and show that mapping and positional cloning efforts in different lepidopteran species can be reciprocally informative.

Ecological speciation without host plant specialization; possible origins of a recently described crypticPapiliospecies

AbstractNorth AmericanPapilio canadensisandP. glaucus(Lepidoptera: Papilionidae, thesePapilio = Pterourus) have previously been described as having allopatric distributions separated by a narrow hybrid zone running from Minnesota to southern New England, and southward in the Appalachian Mountains (possibly to northern Georgia). Recent patterns of hybridization and introgression suggest a more complex interaction between the two, possibly even resulting in the formation of a new species (Pterourus appalachiensisPavulaan & Wright, 2002). Recently, extensive northward interspecific introgression ofP. glaucus‐diagnostic traits has been observed in the hybrid zone. These include wing bands and other color patterns, the ability to feed on tulip tree leaves, andHk‐100allozymes; all are autosomally encoded. However, there has been little northward introgression of certain otherP. glaucustraits (such as facultative diapause and bivoltinism, andLdh‐100allozymes, both X‐linked; and the Y‐linked melanic mimicry gene in females). Interspecific recombination of the X‐chromosome has evidently occurred, as shown by discordant patterns of X‐linked markers. TheP. glaucusX‐linkedPgd‐100andPgd‐50alleles have introgressed 200–400 km north of the historical hybrid zone, yet theP. glaucusX‐linkedLdh‐100allele has not. The allele frequency shift for both genes is more closely related to the ‘thermal landscape’ (i.e., accumulated degree‐days above a developmental base threshold of 50 °F (=10 °C)) than to latitude. Delayed post‐diapause eclosion of cohorts within the hybrid zone, e.g., the New York/Vermont border area, has produced a natural ‘false‐second generation’ flight (a hybrid swarm of synchronous males and females, where 2300–2700 °F degree‐days have accumulated each year since 1998) that is reproductively isolated from flights of both parental species. Moreover, the newly describedP. appalachiensisexhibits a unique combination of traits. These include obligate diapause, a univoltine habit, and theLdh‐80orLdh‐40alleles (as forP. canadensis), thePgd‐100orPgd‐50alleles (as forP. glaucus), and a delayed ‘false‐second generation’ reproductive flight period (as observed in the hybrid zone). Since 2001, a rare allele or ‘hybrizyme’ (Ldh‐20) has appeared in this false second generation at high frequencies (40–50%). We hypothesize that strong selection against the facultative diapause (od‐)trait (and the linkedLdh‐100allele) in regions with 2800 °F degree‐days or less, and divergent selection in favor ofPgd‐100(or a closely linked trait) combined with allochronic reproductive isolation, has resulted in recombinational, parapatric, hybrid speciation. There is no evidence at present that host‐plant shifts or changes in sex pheromones have driven this process, in contrast to many other speciation events in the Lepidoptera.

Theoretical genetics of batesian mimicry III. Evolution of dominance

This paper presents the results of simulating two-locus systems with Batesian mimicry, with special reference to the evolution of dominance. Systems with a single model, and with two species of models, and their mimics are considered. With one species of model, it is shown that either dominance or recessivity of an original mimicry gene may evolve, depending on the equilibrium state that is reached before the modifier mutation occurs. Using this system, we offer a possible explanation for the recessiveness of the mimicry gene in the Abyssinian population of Papilio dardanus. With two species of model, the system becomes too complex to draw more than partial conclusions, and it seems unlikely that considerations of dominance modifiers alone are a sufficiently informative basis for firm prediction.

Theoretical genetics of batesian mimicry II. Evolution of supergenes

In this paper, we describe an extension of the computer model explained in paper I to simulate the genetics of two loci, and have used it to study the selection of genes modifying the effects of mimicry genes, either by improving the mimicry towards the same model, or by giving some mimetic resemblance to a new model. The results suggest a possible explanation of the phenomenon of imperfect mimicry. They also predict that, as appears to be the case in Papilio dardanus, populations will either become fixed for the mimicry gene or else eliminate any non-specific modifiers that are not extremely closely linked to the mimicry locus. This leads us to a consideration of the evolution of mimicry supergenes, which we conclude is unlikely to have occurred by means of unlinked or loosely-linked genes being brought together into one region of the chromosome.