Social antagonism facilitates supergene expansion in ants
Social antagonism facilitates supergene expansion in ants
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DOI：
10.1016/j.cub.2023.10.049
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发表时间：
2023-12-04
期刊：
影响因子：
9.2
通讯作者：
Purcell，Jessica
中科院分区：
文献类型：
--
作者：
Scarparo，Giulia;Palanchon，Marie;Purcell，Jessica
长期以来，拮抗选择一直被认为是性染色体形成和扩大的主要驱动力。例如，常染色体上的性别拮抗变异可以选择抑制该常染色体和性染色体之间的重组，从而产生新的性染色体。常染色体超基因，即含有影响相同复杂性状的紧密连锁变异的染色体区域，与性染色体有相似之处，这增加了性染色体进化模型可以解释基因组结构进化和其他背景下重组的可能性。我们在一个前驱虫物种中测试了这一前提，在该物种中，我们在3号染色体上鉴定了4种超基因单倍型，这些单倍型与群体社会组织和性别比例有关。我们在9号染色体上发现了一个新的重排超基因变体(9r)，这是女王小型化的基础。9R与多皇后群体中发现的一个3号染色体单倍型(P2)存在强连锁不平衡。我们认为，女王小型化在单一女王(一夫一妻)的背景下是非常不受欢迎的，因此是社会对立的。因此，生活在不同的社会环境中的蚂蚁经历的不同选择可能是导致9号染色体上的遗传多态和相关的女王大小二型性出现的原因之一。因此，一种与多倍体相关的祖先单倍型可能已经扩展到包括9号染色体上的多态，导致跨越两条染色体的更大的抑制重组区域。这一过程类似于新性染色体的形成，并与抑制重组的扩张区模型一致。我们认为，小型蜂王比没有9R的蜂王小16%-20%，可能是早期的种内社会寄生虫。
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 aFormicaant 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 is 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.