Supergene genotypes and associated phenotypes in Formica cinerea samples

Antagonistic selection has long been considered a major driver of the
formation and expansion of sex chromosomes. For example, sexually
antagonistic variation on an autosome can select for suppressed
recombination between that autosome and the sex chromosome, leading to a
neo-sex chromosome. Autosomal supergenes, chromosomal regions containing
tightly linked variants affecting the same complex trait, share
similarities with sex chromosomes, raising the possibility that sex
chromosome evolution models can explain the evolution of genome structure
and recombination in other contexts.  We tested this
premise in a Formica ant species wherein we identified
four supergene haplotypes on chromosome 3 underlying colony social
organization and sex ratio. We discovered a novel rearranged supergene
variant (9r) on chromosome 9 underlying queen miniaturization. The 9r is
in strong linkage disequilibrium with one chromosome 3 haplotype (P2)
found in multi-queen (polygyne) colonies. We suggest that queen
miniaturization is strongly disfavored in the single queen (monogyne)
background, and thus socially antagonistic. As such, divergent selection
experienced by ants living in alternative social ‘environments’ (monogyne
and polygyne) may have contributed to the emergence of a genetic
polymorphism on chromosome 9 and associated queen-size dimorphism.
Consequently, an ancestral polygyne-associated haplotype may have expanded
to include the polymorphism on chromosome 9, resulting in a larger region
of suppressed recombination spanning two chromosomes. This process is
analogous to the formation of neo-sex chromosomes and consistent with
models of expanding regions of suppressed recombination. We propose that
miniaturized queens, 16-20% smaller than queens without 9r, could be
incipient intraspecific social parasites.

拮抗选择（antagonistic selection）长期以来被视作性染色体（sex chromosomes）形成与扩张的核心驱动因素。例如，常染色体（autosome）上的性拮抗变异可通过选择作用抑制该常染色体与性染色体之间的重组，进而催生新性染色体（neo-sex chromosome）。常染色体超基因（autosomal supergenes）指染色体上包含调控同一复杂性状的紧密连锁变异的区域，其与性染色体存在诸多相似性，这提示性染色体演化模型或可解释其他场景下的基因组结构与重组演化规律。

我们在一种林蚁属（Formica）蚂蚁类群中验证了这一假说：研究人员在该类群的3号染色体上鉴定出4种超基因单倍型，这些单倍型是蚁群社会组织结构与性比的调控基础。我们还在9号染色体上发现了一种全新的重排超基因变异体（9r），该变异与蚁后体型小型化直接相关。

9r变异体与多蚁后（polygyne）蚁群中存在的3号染色体单倍型（P2）存在极强的连锁不平衡（linkage disequilibrium）。我们推测，在单蚁后（monogyne）的社会背景下，蚁后体型小型化会受到强烈的选择排斥，因此属于社会拮抗性状。换言之，生存于单蚁后与多蚁后这两种不同社会“环境”中的蚂蚁所经历的歧化选择（divergent selection），可能推动了9号染色体上遗传多态性的产生，并伴随出现蚁后体型二态性。

因此，一种与多蚁后社会型相关的祖先单倍型或许发生了扩张，纳入了9号染色体上的多态性区域，最终形成了覆盖两条染色体的更大范围的重组抑制区域。这一过程与新性染色体的形成过程高度类似，也符合重组抑制区域扩张的演化模型。我们提出，携带9r变异的小型化蚁后（体型较无该变异的蚁后小16%~20%）可能正处于种内社会寄生者的演化初期阶段。