Naturalis Biodiversity Center, PO Box 9517, 2300 RA, Leiden, The Netherlands.
Institute of Biology Leiden, Leiden University, PO Box 9505, 2300 RA, Leiden, The Netherlands.
Philos Trans R Soc Lond B Biol Sci. 2022 Aug;377(1856):20210199. doi: 10.1098/rstb.2021.0199. Epub 2022 Jun 13.
Supergenes offer spectacular examples of long-term balancing selection in nature, but their origin and maintenance remain a mystery. Reduced recombination between arrangements, a critical aspect of many supergenes, protects adaptive multi-trait phenotypes but can lead to mutation accumulation. Mutation accumulation can stabilize the system through the emergence of associative overdominance (AOD), destabilize the system, or lead to new evolutionary outcomes. One outcome is the formation of maladaptive balanced lethal systems, where only heterozygotes remain viable and reproduce. We investigated the conditions under which these different outcomes occur, assuming a scenario of introgression after divergence. We found that AOD aided the invasion of a new supergene arrangement and the establishment of a polymorphism. However, this polymorphism was easily destabilized by further mutation accumulation, which was often asymmetric, disrupting the quasi-equilibrium state. Mechanisms that accelerated degeneration tended to amplify asymmetric mutation accumulation between the supergene arrangements and vice-versa. As the evolution of balanced lethal systems requires symmetric degeneration of both arrangements, this leaves only restricted conditions for their evolution, namely small population sizes and low rates of gene conversion. The dichotomy between the persistence of polymorphism and degeneration of supergene arrangements likely underlies the rarity of balanced lethal systems in nature. This article is part of the theme issue 'Genomic architecture of supergenes: causes and evolutionary consequences'.
超基因为自然中长期平衡选择提供了引人注目的例子，但它们的起源和维持仍然是一个谜。排列之间重组的减少是许多超基因的一个关键方面，它保护了适应性多性状表型，但可能导致突变积累。突变积累可以通过关联超显性（AOD）的出现稳定系统，也可以破坏系统，或者导致新的进化结果。一种结果是形成适应性平衡致死系统，其中只有杂合子仍然具有活力并繁殖。我们研究了在假设分歧后基因渐渗情景下，这些不同结果发生的条件。我们发现，AOD 有助于新的超基因排列的入侵和多态性的建立。然而，这种多态性很容易被进一步的突变积累破坏，而这种积累往往是不对称的，破坏了准平衡状态。加速退化的机制往往会加剧超基因排列之间的不对称突变积累，反之亦然。由于平衡致死系统的进化需要两个排列的对称退化，因此它们的进化只有在有限的条件下才能进行，即小种群大小和低基因转换率。多态性持续和超基因排列退化之间的二分法可能是平衡致死系统在自然界中罕见的原因。本文是主题为“超级基因的基因组结构：原因和进化后果”的一部分。
