The genetic architecture of adaptation: convergence and pleiotropy in Heliconius wing pattern evolution.

Unravelling the genetic basis of adaptive traits is a major challenge in evolutionary biology. Doing so informs our understanding of evolution towards an adaptive optimum, the distribution of locus effect sizes, and the influence of genetic architecture on the evolvability of a trait. In the Müllerian co-mimics Heliconius melpomene and Heliconius erato some Mendelian loci affecting mimicry shifts are well known. However, several phenotypes in H. melpomene remain to be mapped, and the quantitative genetics of colour pattern variation has rarely been analysed. Here we use quantitative trait loci (QTL) analyses of crosses between H. melpomene races from Peru and Suriname to map, for the first time, the control of the broken band phenotype to WntA and identify a ~100 kb region controlling this variation. Additionally, we map variation in basal forewing red-orange pigmentation to a locus centred around the gene ventral veins lacking (vvl). The locus also appears to affect medial band shape variation as it was previously known to do in H. erato. This adds to the list of homologous regions controlling convergent phenotypes between these two species. Finally we show that Heliconius wing-patterning genes are strikingly pleiotropic among wing pattern traits. Our results demonstrate how genetic architecture can shape, aid and constrain adaptive evolution.

Morris J ，Navarro N ，Rastas P ，Rawlins LD ，Sammy J ，Mallet J ，Dasmahapatra KK ... -  《-》

Conservatism and novelty in the genetic architecture of adaptation in Heliconius butterflies.

Huber B ，Whibley A ，Poul YL ，Navarro N ，Martin A ，Baxter S ，Shah A ，Gilles B ，Wirth T ，McMillan WO ，Joron M ... -  《-》

Comparative population genetics of a mimicry locus among hybridizing Heliconius butterfly species.

The comimetic Heliconius butterfly species pair, H. erato and H. melpomene, appear to use a conserved Mendelian switch locus to generate their matching red wing patterns. Here we investigate whether H. cydno and H. pachinus, species closely related to H. melpomene, use this same switch locus to generate their highly divergent red and brown color pattern elements. Using an F2 intercross between H. cydno and H. pachinus, we first map the genomic positions of two novel red/brown wing pattern elements; the G locus, which controls the presence of red vs brown at the base of the ventral wings, and the Br locus, which controls the presence vs absence of a brown oval pattern on the ventral hind wing. The results reveal that the G locus is tightly linked to markers in the genomic interval that controls red wing pattern elements of H. erato and H. melpomene. Br is on the same linkage group but approximately 26 cM away. Next, we analyze fine-scale patterns of genetic differentiation and linkage disequilibrium throughout the G locus candidate interval in H. cydno, H. pachinus and H. melpomene, and find evidence for elevated differentiation between H. cydno and H. pachinus, but no localized signature of association. Overall, these results indicate that the G locus maps to the same interval as the locus controlling red patterning in H. melpomene and H. erato. This, in turn, suggests that the genes controlling red pattern elements may be homologous across Heliconius, supporting the hypothesis that Heliconius butterflies use a limited suite of conserved genetic switch loci to generate both convergent and divergent wing patterns.

Chamberlain NL ，Hill RI ，Baxter SW ，Jiggins CD ，Kronforst MR ... -  《-》

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

With 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. Scoring 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. Here 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.

Papa R ，Morrison CM ，Walters JR ，Counterman BA ，Chen R ，Halder G ，Ferguson L ，Chamberlain N ，Ffrench-Constant R ，Kapan DD ，Jiggins CD ，Reed RD ，McMillan WO ... -  《BMC GENOMICS》

Convergent evolution in the genetic basis of Müllerian mimicry in heliconius butterflies.

The neotropical butterflies Heliconius melpomene and H. erato are Müllerian mimics that display the same warningly colored wing patterns in local populations, yet pattern diversity between geographic regions. Linkage mapping has previously shown convergent red wing phenotypes in these species are controlled by loci on homologous chromosomes. Here, AFLP bulk segregant analysis using H. melpomene crosses identified genetic markers tightly linked to two red wing-patterning loci. These markers were used to screen a H. melpomene BAC library and a tile path was assembled spanning one locus completely and part of the second. Concurrently, a similar strategy was used to identify a BAC clone tightly linked to the locus controlling the mimetic red wing phenotypes in H. erato. A methionine rich storage protein (MRSP) gene was identified within this BAC clone, and comparative genetic mapping shows red wing color loci are in homologous regions of the genome of H. erato and H. melpomene. Subtle differences in these convergent phenotypes imply they evolved independently using somewhat different developmental routes, but are nonetheless regulated by the same switch locus. Genetic mapping of MRSP in a third related species, the "tiger" patterned H. numata, has no association with wing patterning and shows no evidence for genomic translocation of wing-patterning loci.

Baxter SW ，Papa R ，Chamberlain N ，Humphray SJ ，Joron M ，Morrison C ，ffrench-Constant RH ，McMillan WO ，Jiggins CD ... -  《GENETICS》