Data from: The role of breakpoint mutations, supergene effects, and ancient nested rearrangements in the evolution of adaptive chromosome inversions in the yellow monkey flower, Mimulus guttatus

Large chromosomal inversion polymorphisms are ubiquitous across the
diversity of diploid organisms and play a large role in the evolution of
adaptations in those species. Despite their importance, the underlying
mechanisms by which inversions produce their adaptive phenotypic effects
and become geographically widespread are still poorly understood. One way
inversions could cause phenotypic effects is through meiotic recombination
suppression, which can result in the formation of a supergene containing
linked adaptive alleles. This supergene hypothesis has been promoted by
theoreticians, but thus far, no studies have definitively identified
multiple linked adaptive genes within an inversion. Alternatively,
according to the breakpoint mutation hypothesis, the inversion mutation
itself could result in adaptive phenotypic effects if it disrupts genes or
alters the regulation of nearby genes. Here, we evaluate both of these
hypotheses using new long-read sequencing-based genomes of the yellow
monkey flower, Mimulus guttatus. Our results provide support for
both the supergene and breakpoint mutation hypotheses of adaptive
inversion evolution and suggest that functional molecular studies will be
required to definitively test each of these hypotheses. We also identified
an ancient large inversion nested within a well-established adaptive
inversion. This finding suggests that the supergene mechanism may occur in
phases, with an expansion of the region of suppressed recombination
capturing an increasing number of adaptive loci over time.

大型染色体倒位多态性（large chromosomal inversion polymorphisms）在各类二倍体生物中普遍存在，并对这些物种的适应性演化具有重要作用。尽管其重要性不言而喻，但倒位产生适应性表型效应并实现地理扩散的潜在机制，目前仍未得到充分阐释。倒位引发表型效应的潜在途径之一，是通过减数分裂重组抑制（meiotic recombination suppression），该过程可形成包含连锁适应性等位基因的超基因（supergene）。这一超基因假说已得到理论学界的支持，但迄今为止尚无研究能够在倒位区域内明确鉴定出多个连锁的适应性基因。另一种备选假说为断点突变假说（breakpoint mutation hypothesis）：若倒位突变本身破坏了基因序列或改变了邻近基因的调控模式，即可产生适应性表型效应。本研究借助基于长读长测序（long-read sequencing）获得的黄色猴面花（Mimulus guttatus）全新基因组数据，对上述两种假说进行了验证。本研究结果既为适应性倒位演化的超基因假说与断点突变假说提供了支持，同时也提示，需开展功能性分子研究才能对这两种假说分别做出确定性验证。我们还在一处已被广泛证实的适应性倒位内部，鉴定出了一处古老的大型倒位。这一发现表明，超基因机制可能以阶段性方式运作：随着时间推移，重组抑制区域不断扩张，其所捕获的适应性基因座数量也随之增加。