Recombination within the<i>Cepaea nemoralis</i>supergene is confounded by incomplete penetrance and epistasis

Davison, Angus; Gonzalez, Daniel Ramos; Aramendia, Amaia Caro

doi:10.1101/472456

Cited by 6 publications

(7 citation statements)

References 19 publications

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“…However, while much is known about among‐morph variation in thermal tolerance, life history, physiology (Kavaliers, 1992; Kerstes et al, 2019; Lamotte, 1959; Oosterhoff, 1977; Richardson, 1974; Tilling, 1983; Wolda, 1967), we know nothing, as far as we can tell, about within‐morph, but among‐genotype variation. Investigations using individuals of known genotype obtained through repeated crosses or, as our knowledge of the actual molecular underpinnings increases, through direct genotyping (Gonzalez et al, 2019; Kerkvliet et al, 2017), may shed light on this “hidden” genetic variation and whether it contributes to the persistence of morph‐related behavior differences.…”

Section: Discussionmentioning

confidence: 99%

Boldness and exploration vary between shell morphs but not environmental contexts in the snail Cepaea nemoralis

2021

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Understanding the maintenance of among‐individual behavioral variation in populations and predicting its consequences are key challenges in behavioral ecology. Studying the association between repeatable behaviors and other traits under selection may shed light on the underlying selective pressures. We used the model snail Cepaea nemoralis to examine whether individual behavior is associated with shell morph, a key trait that has been extensively studied in the context of thermal tolerance and predator avoidance, and which is known to be under strict genetic control in this species. We quantified proxies of boldness and exploration in snails of three morphs coming from two habitats with different thermal contexts. We show that both behaviors were repeatable at the among‐individual level (within‐state Rboldness = 0.22 [95% credible interval: 0.15; 0.29]; Rexploration = 0.20 [0.15; 0.25]). Behavior was associated with shell morph, with the darker morph (five‐banded) being consistently shyer and slower to explore. There was no evidence that thermal environment of origin influenced behavior. Snails became faster when test temperature increased; we found no evidence morphs differed in their thermal response. Boldness and exploration were correlated among individuals, forming a syndrome (r = 0.28 [0.10; 0.46]). The link we find between morph and boldness is compatible with visual selection by avian predators, assuming a positive association between boldness and morphological defense (phenotypic compensation hypothesis). The fact morph‐behaviors associations are consistent across environments, despite selection on morph, hint to a possible underlying genetic origin. Finally, we discuss how our findings combined with decades of evolutionary research make C. nemoralis a very valuable model to study the evolution of behavior in response to environmental changes.

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Section: Discussionmentioning

confidence: 99%

Boldness and exploration vary between shell morphs but not environmental contexts in the snail Cepaea nemoralis

2021

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“…3, a continuum of situations can be observed, characterised by variations in the importance of migration in the maintenance of polymorphism. We consider the term supergene is most useful to describe the genetic architectures which facilitate the maintenance of polymorphism and the segregation of discrete forms (15), as in most of the classic cases on distyly, mimicry, shell morphologies, or behavioral syndromes (6, 8–11, 34, 45). Those tend to be cases with known or suspected epistasy among linked loci as well as some level of overdominance, and represent one end of the spectrum predicted by our model (case represented in Fig.…”

Section: Discussionmentioning

confidence: 99%

“…Known supergenes are nearly always associated with obvious color polymorphism (e.g. (7–9, 11, 12, 17); This is likely a detection bias and current advances in sequencing technology could thus reveal the presence of such architecture coding a wide diversity of traits in numerous species.…”

Section: Discussionmentioning

confidence: 99%

“…Discrete polymorphisms are widespread in nature. Besides the ubiquitous polymorphism of sexual and mating types (1, 2), classic examples of discrete polymorphisms involving multiple functional loci include polymorphic immune systems in vertebrates (3–5), and color polymorphisms in several birds (6–8), insects (9, 10), snails (11, 12) and lizards (13). Supergenes are genetic architectures which are often found to underlie discrete polymorphisms by preventing the formation of intermediate maladapted phenotypes.…”

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Admixture can readily lead to the formation of supergenes

Jay

Aubier

Joron

2020

Preprint

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Supergenes are genetic architectures allowing the segregation of alternative combinations of alleles underlying complex phenotypes. The co-segregation of sets of alleles at linked loci is determined by polymorphic chromosomal rearrangements suppressing recombination locally. Supergenes are involved in many complex polymorphisms, including sexual, color or behavioral polymorphisms in numerous plants, fungi, mammals, fish, and insects. Despite a long history of empirical and theoretical research, the genetic origin of supergenes remains poorly understood. Here, using a population genetic two-island model, we explore how the evolution of overdominant chromosomal inversions may lead to the formation of supergenes. We show that the evolution of inversions in differentiated populations connected by gene flow leads to an increase in frequency of poorly adapted, immigrant haplotypes. When inversions are associated with recessive fitness cost hampering their fixation (such as a mutational load), this results in the formation of supergenes. These results provide a realistic scenario for the evolution of supergenes and inversion polymorphisms in general, and bring new light into the importance of admixture in the formation of new genetic architectures.

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“…A revision of the classic genetic model also occurred for the iconic land snail Cepaea nemoralis (Table 1), where cryptic shell colour‐pattern was long thought to be associated with five loci locked within an inversion (Cain & Sheppard, 1954). Recent work showed an absence of recombination in the putative supergene, casting doubt on the number and linkage relationships of loci controlling shell colour (Gonzalez et al, 2019). These recent developments urge for more rigorous tests on the true number of selected variants within supergenes and their precise genomic location(s).…”

Section: The Supergene Hypothesis: What Is the Evidence For Recombination Suppression Among Loci Controlling Selected Trait Variation?mentioning

confidence: 99%

Inversion breakpoints and the evolution of supergenes

et al. 2021

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The coexistence of discrete morphs that differ in multiple traits is common within natural populations of many taxa. Such morphs are often associated with chromosomal inversions, presumably because the recombination suppressing effects of inversions help maintain alternate adaptive combinations of alleles across the multiple loci affecting these traits. However, inversions can also harbour selected mutations at their breakpoints, leading to their rise in frequency in addition to (or independent from) their role in recombination suppression. In this review, we first describe the different ways that breakpoints can create mutations. We then critically examine the evidence for the breakpoint‐mutation and recombination suppression hypotheses for explaining the existence of discrete morphs associated with chromosomal inversions. We find that the evidence that inversions are favoured due to recombination suppression is often indirect. The evidence that breakpoints harbour mutations that are adaptive is also largely indirect, with the characterization of inversion breakpoints at the sequence level being incomplete in most systems. Direct tests of the role of suppressed recombination and breakpoint mutations in inversion evolution are thus needed. Finally, we emphasize how the two hypotheses of recombination suppression and breakpoint mutation can act in conjunction, with implications for understanding the emergence of supergenes and their evolutionary dynamics. We conclude by discussing how breakpoint characterization could improve our understanding of complex, discrete phenotypic forms in nature.

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Recombination within theCepaea nemoralissupergene is confounded by incomplete penetrance and epistasis

Cited by 6 publications

References 19 publications

Boldness and exploration vary between shell morphs but not environmental contexts in the snail Cepaea nemoralis

Boldness and exploration vary between shell morphs but not environmental contexts in the snail Cepaea nemoralis

Admixture can readily lead to the formation of supergenes

Inversion breakpoints and the evolution of supergenes

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