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Recombination Within the Cepaea Nemoralis Supergene Is Confounded by Incomplete Penetrance and Epistasis

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Recombination Within the Cepaea Nemoralis Supergene Is Confounded by Incomplete Penetrance and Epistasis Heredity (2019) 123:153–161 https://doi.org/10.1038/s41437-019-0190-6 ARTICLE Recombination within the Cepaea nemoralis supergene is confounded by incomplete penetrance and epistasis 1 1,2 1 Daniel Ramos Gonzalez ● Amaia Caro Aramendia ● Angus Davison Received: 19 November 2018 / Revised: 9 January 2019 / Accepted: 13 January 2019 / Published online: 14 February 2019 © The Author(s) 2019. This article is published with open access Abstract Although the land snail Cepaea nemoralis is one of the most thoroughly investigated colour polymorphic species, there have been few recent studies on the inheritance of the shell traits. Previously, it has been shown that the shell polymorphism is controlled by a series of nine or more loci, of which five make a single ‘supergene’ containing tightly linked colour and banding loci and more loosely linked pigmentation, spread band and punctate loci. However, one limitation of earlier work was that putative instances of recombination between loci within the supergene were not easily verified. We therefore generated a new set of C. nemoralis crosses that segregate for colour, banding and pigmentation, and several other unlinked shell phenotype loci. The snails were genotyped using a set of RAD-seq-derived loci that flank the supergene, and instances 1234567890();,: 1234567890();,: of recombination tested by comparing inferred supergene genotype against RAD-marker genotype. We found no evidence that suspected ‘recombinant’ individuals are recombinant between loci within the supergene. As point estimates of recombination between both colour/banding, and colour/pigmentation loci are zero, incomplete penetrance and epistasis are a better explanation for the apparent ‘recombinant’ phenotype of some snail shells. Overall, this work, therefore, shows that the architecture of the supergene may not be as previously supposed. It also provides a resource for fine mapping of the supergene and other major shell phenotype loci. Introduction benefit that the major loci that determine the polymorphism show simple Mendelian inheritance (Cook 1967; Jones Historically, some of the most important animals in study- et al. 1977). However, while ongoing and long-term studies ing colour polymorphism have been the land snails Cepaea on these animals continue to provide compelling evidence nemoralis and the sister taxon, C. hortensis, because it is for the fundamental role of natural selection in promoting straightforward to collect them and record the frequencies and maintaining variation in natural populations, as well as of the different morphs in different locations and habitats the impact of modern-day habitat change (Cameron and (Cain and Sheppard 1950; Cain and Sheppard 1952; Cain Cook 2012; Cook 2017; Silvertown et al. 2011), the last and Sheppard 1954; Jones et al. 1977). There is also the research on the inheritance of the loci that determine the polymorphism dates to the late 1960s. This is a problem because now that there is finally some progress towards identifying the genes involved (Kerkvliet et al. 2017; Mann These authors contributed equally: Daniel Ramos Gonzalez, Amaia Caro Aramendia and Jackson 2014; Richards et al. 2013), it is important that laboratory crosses are available, to validate prior knowledge Supplementary information The online version of this article (https:// on the inheritance and for use in fine mapping recombina- doi.org/10.1038/s41437-019-0190-6) contains supplementary material, which is available to authorized users. tion break-points. Previous work has shown that the shell polymorphism is * Angus Davison controlled by a series of nine or more loci, of which five or [email protected] more make a single ‘supergene’, containing linked C B 1 School of Life Sciences, University of Nottingham, shell ground colour ( ), banding ( ), band/lip pigmentation Nottingham NG7 2RD, UK (P/L), spread band (S) and punctate (or ‘interrupted’; I) loci. 2 Departamento de Zoología y Biología Celular Animal, In most studies, colour and banding have been found to be Universidad del País Vasco, Paseo Univ 7, Vitoria 01006, Spain tightly linked, with recombination typically towards the 154 D.aniel R.amos Gonzalez et al. lower end of 0–2% (Cain et al. 1960; Cook 1967; Cook and raised to adulthood in isolation and then introduced to a King 1966). The exceptions are a study by Fisher and Diver partner. Pairs of snails were then kept in tanks with ~4 cm (1934), which reported recombination of ~20% between C/ soil until egg laying began. As C. nemoralis is a simulta- B, and two crosses in Cain et al. (1960) which showed neous hermaphrodite, offspring from both parents were recombination of ~16%, also between C/B. Although there used. Egg batches were isolated, and the offspring reared to have been fewer studies, pigmentation, spread band and adulthood under the same feeding regime, with the time punctate are believed more loosely linked, showing rates of from egg to adult being ~6 months. Parents and adult off- recombination between 3 and 15% (Cain et al. 1960; Cain spring, or large subadult offspring were preserved frozen. et al. 1968; Cook 1967). The main other loci that make up The majority of snails were raised to adulthood, and so the shell phenotype are various forms of band-suppressing the colour, banding, band pigmentation and lip colour loci, all unlinked to the supergene, including the mid-band phenotype was scored and then the shell genotype inferred. locus, U (unifasciata), and another that suppresses the first Complications in scoring some characters necessitated two bands, T (trifasciata). minor deviations from the scheme put forward by Cain One unavoidable limitation of prior works was that (1988), summarised in Table 1. To distinguish phenotype putative instances of recombination between loci within the from genes and genotypes, symbols for the latter are in supergene could not be verified, except by breeding further italics. generations of snails from the ‘recombinant’ offspring to We have previously shown that colour variation is confirm the underlying genotype. This was rarely possible, multimodal but continuously variable in natural popula- perhaps due to logistics combined with the fact that many tions, necessitating the use of quantitative methods to pairs do not produce offspring. Nonetheless, it was recog- measure it (Davison et al. 2018). However, in simple nised that incomplete penetrance might be an alternative crosses it is straightforward to bin the individuals into one explanation for the phenotype of recombinants. Chance of two types; quantitative measures are not necessary. arrangements of alleles at other loci might sometimes Therefore, the shell ground colour phenotype was scored as interact to prevent expression of a particular phenotype, either yellow (Y), pink (P) or brown (B), and where pos- causing individuals to appear as if they are ‘recombinant’ sible, the corresponding genotype inferred (dominance is (Cook and King 1966). CB > CP > CY), including whether in coupling or repulsion To further understand the frequency of recombination phase with other loci (Table 1). within the supergene, and to generate further material for Similarly, banding phenotype was generally scored as fine mapping, we made a new set of C. nemoralis crosses either unbanded (O; 00000), mid-banded (M; 00300) or that segregate for several shell phenotype loci. The off- having several bands (B; most frequently 12345, but all spring were then genotyped using a set of linked RAD-seq combinations except 00300) and the genotype at the banding loci that flank either side of the supergene (Richards et al. locus was inferred (unbanded dominant; BO > BB). Several 2013), and instances of recombination confirmed or refuted crosses also segregated for the mid-band locus, so the gen- by comparing inferred supergene genotype against RAD- otype at that locus was also inferred (mid-band dominant; marker genotype. The underlying idea is that individuals U3 > U-). One cross potentially segregated for two other that show recombination within the supergene should also band-suppressing loci, T (first two bands missing: 00345; be recombinant by RAD-marker. Overall, we found that the T345 > T-) and another possible locus, which we called X phenotype of ‘recombinant’ individuals is better explained (first band missing or very faint: 02345; X2345 >X-). by incomplete penetrance and epistasis. It is not clear from previous studies as to whether the lip This work, therefore, provides a method to identify pigmentation is a separate locus, or is instead allelomorphic recombination events that either flank the supergene or are with the band pigmentation locus. As a precaution, the two between loci within the supergene. The results also show were therefore treated separately. Thus, band pigmentation that recombination within the supergene may be con- phenotype was scored as normal (N) or hyalozonate (H) and siderably rarer than supposed. the corresponding genotype inferred (PN > PH). Hyalozonate shells typically have unpigmented bands and lip (see Dis- cussion); discrete bands can still be recognised because the Materials and methods background colour is paler than the shell ground colour. In some crosses, the lip pigmentation phenotype was The culture of Cepaea two distinct types, either normal (L), or white lip (A; albolabiate), and so the corresponding genotype was infer- Snails were fed a hydrated grass pellet, oat and chalk mix, red (LL > LA). In other crosses, lip pigmentation showed supplemented with lettuce, as described
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