Department of Entomology, University of California, Riverside, 165 Entomology Bldg. Citrus Drive, Riverside, CA 92521, USA.
Department of Evolution, Ecology, and Organismal Biology, University of California, Riverside, 2710 Life Science Bldg., Riverside, CA 92521, USA.
Curr Biol. 2023 Dec 4;33(23):5085-5095.e4. doi: 10.1016/j.cub.2023.10.049. Epub 2023 Nov 17.
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 (P) 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.
拮抗选择长期以来被认为是形成和扩展性染色体的主要驱动力。例如，常染色体上的性拮抗变异可以选择抑制该常染色体与性染色体之间的重组，从而导致新的性染色体。常染色体超基因，包含紧密连锁的影响同一复杂性状的变体的染色体区域，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其他背景下基因组结构和重组进化的可能性。我们在一种 Formica 蚂蚁物种中检验了这一前提，在该物种中，我们确定了控制群体社会组织和性别比例的 3 号染色体上的四个超基因单倍型。我们发现了 9 号染色体上一个新的重排超基因变体（9r），它与多皇后（polygyne）群体中发现的 3 号染色体单倍型（P）紧密连锁。我们认为，在单皇后（monogyne）背景下，女王微型化受到强烈的不利影响，因此在社会上是拮抗的。因此，生活在不同社会“环境”（单皇后和多皇后）中的蚂蚁所经历的分歧选择可能导致了 9 号染色体上遗传多态性的出现以及相关的女王大小二态性。因此，一个与祖先多皇后相关的单倍型可能已经扩展到包括 9 号染色体上的多态性，导致跨越两个染色体的抑制重组的更大区域。这个过程类似于新性染色体的形成，与抑制重组区域扩张的模型一致。我们提出，与没有 9r 的女王相比，缩小 16%-20%的微型女王可能是新出现的种内社会性寄生虫。
