Genetic convergence of industrial melanism in three geometrid moths

Abstract

The rise of dark (melanic) forms of many species of moth in heavily coal-polluted areas of nineteenth- and twentieth-century Britain, and their post-1970s fall, point to a common selective pressure (camouflage against bird predators) acting at the community level. The extent to which this convergent phenotypic response relied on similar genetic and developmental mechanisms is unknown. We examine this problem by testing the hypothesis that the locus controlling melanism in Phigalia pilosaria and Odontopera bidentata, two species of geometrid moth that showed strong associations between melanism and coal pollution, is the same as that controlling melanism in Biston betularia, previously identified as the gene cortex. Comparative linkage mapping using family material supports the hypothesis for both species, indicating a deeply conserved developmental mechanism for melanism involving cortex. However, in contrast to the strong selective sweep signature seen in British B. betularia, no significant association was detected between cortex-region markers and melanic morphs in wild-caught samples of P. pilosaria and O. bidentata, implying much older, or diverse, origins of melanic morph alleles in these latter species.

Keywords: Lepidoptera; cortex; melanism; parallel evolution.

Figure 1.

(a) Melanic polymorphism in Biston betularia, Phigalia pilosaria and Odontopera bidentata. Lighter and darker forms of insularia than the one shown exist. For O. bidentata, typica-1 is more common in southern England, whereas typica-2 prevails in the northwest region. The different species are scaled to similar size. Photographs from Natural History Museum Data Portal [19]. (b) Frequency of melanics in three moth species on a cline from west N. Wales to Cheshire and Lancashire, east of Manchester, during the period of high melanic frequency (late 1960s–mid 1970s). For P. pilosaria, the totals in both melanic classes (monacharia and intermediate) are shown. Map of transect in [20]. (Data from [,,–23]).

Figure 2.

(a) Genomic positions, on a centimorgan scale, of the loci controlling typical–melanic polymorphism in P. pilosaria (monacharia), B. betularia (carbonaria) and O. bidentata (nigra), relative to gene orthologues (connected by lines). (b) Relevant genic content (11 of 56 genes) within this chromosomal region, and the position of the six genetic markers (loci a–e, and cortex exon 1) used to test genotype–phenotype associations in wild samples. Distances are based on B. betularia and are defined relative to the polymorphism controlling typica-carbonaria (carb-TE). The furthest extent of the B. betularia cortex region (shaded black) is extended by multiple alternative first exons (only exons 1A and 1C are shown). Locus a coincides with Trehalase 1A for P. pilosaria and O. bidentata, but Trehalase 1B for B. betularia. (Photographs by Arjen van't Hof).