Stabilizing selection maintains exuberant colour polymorphism in the spider Theridion californicum (Araneae, Theridiidae)

Abstract

Genetically controlled colour polymorphisms provide a physical manifestation of the operation of selection and how this can vary according to the spatial or temporal arrangement of phenotypes, or their frequency in a population. Here, we examine the role of selection in shaping the exuberant colour polymorphism exhibited by the spider Theridion californicum. This species is part of a system in which several distantly related spiders in the same lineage, but living in very different geographical areas, exhibit remarkably convergent polymorphisms. These polymorphisms are characterized by allelic inheritance and the presence of a single common cryptic morph and, in the case of T. californicum and its congener the Hawaiian happy-face spider Theridion grallator, numerous rare patterned morphs. We compare population differentiation estimated from colour phenotypic data to differentiation at neutral amplified fragment length polymorphisms (AFLP) loci and demonstrate that the colour polymorphism appears to be maintained by balancing selection. We also examine the patterns of selection in the genome-wide sample of AFLP loci and compare approaches to detecting signatures of selection in this context. Our results have important implications regarding balancing selection, suggesting that selective agents can act in a similar manner across disparate taxa in globally disjunct locales resulting in parallel evolution of exuberant polymorphism.

Molecular population genetics of the melanic plumage polymorphism in Arctic skuas (Stercorarius parasiticus): evidence for divergent selection on plumage colour

“…However, as pairwise F ST for neutral markers (introns) are low and tend towards zero, the power to detect balancing selection is likely to be much lower as the F ST at the locus under investigation will be contained within the variation of the neutral estimate (see Croucher et al . ). Given the finding of divergent selection among populations, one might expect a signal of balancing selection to be present in standard neutrality statistics either in single populations or across all populations.…”

De novo characterization of the gene-rich transcriptomes of two color-polymorphic spiders, Theridion grallator and T. californicum (Araneae: Theridiidae), with special reference to pigment genes

“…unpatterned) morph or a mixture of “Colored” (patterned) morphs. This simple scheme is based upon the fact that in all species studied, the Yellow morph appears to be recessive to all other color morphs [6,9] and a similar scoring scheme has been used previously [8,73]. For T. californicum the “Yellow” pool comprised 20 Yellow individuals and the “Colored” pool 20 individuals of the following morphs defined in Oxford [9]: “Red lines” (n = 6), “Black spot” (2), “Black blob” (2), “White” (1), “Red ring A” (4), “Red ring B” (2), “Red stripe A” (3).…”

“…Two other, distantly related species within the genus Theridion have become of particular interest because they exhibit a spectacular array of color morphs. The Hawaiian happy-face spider Theridion grallator Simon occurs in native forest on four of the Hawaiian islands and displays more than 20 discrete abdominal color patterns [6,7] while Theridion californicum is found along the Pacific coast of North-America and exhibits at least 12 discrete abdominal color patterns [8,9]. The morphs displayed by these species are remarkably similar, and in the case of T. grallator may have evolved repeatedly, subsequent to colonization of each of the Hawaiian islands [10].…”

“…The most common morphs of each species are also convergent with those displayed by Enoplognatha ovata , E. latimana and some other polymorphic species in the Theridiidae. In all species examined there is a common Yellow morph that typically represents 60-70% of any population and that is recessive to all other morphs, with the Colored (patterned) morphs displaying a dominance hierarchy that broadly reflects the extent of pigmentation [3,4,8,9]. The morphs are created from a palette of yellow, red and dark-brown (almost black) pigments laid down on a reflective background of white guanine crystals and all the pigment appears to be ommochrome based [3,12].…”

Unraveling the thread of nature’s tapestry: the genetics of diversity and convergence in animal pigmentation

“…Furthermore, there are multiple promising arthropod systems, in addition to Drosophila and butterflies, that show complex, convergent pigmentation phenotypes that may be amenable to genetic study ( Figure 5). These include happy face spiders (Croucher et al, 2011;Gillespie and Oxford, 1998;Oxford and Gillespie, 2001) and ladybird beetles (Michie et al, 2010(Michie et al, , 2011Tan, 1946).…”