Ecological Advantages and Evolutionary Limitations of Aggregative Multicellular Development

Ecological Advantages and Evolutionary Limitations of Aggregative Multicellular Development
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集体多细胞发育的生态优势和进化限制

DOI:
10.1016/j.cub.2020.08.006
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发表时间:
2020
期刊:
影响因子:
9.2
通讯作者:
Ratcliff, William C.
Ratcliff, William C.
中科院分区:
生物学1区
文献类型:
--
作者:
Pentz, Jennifer T.;Márquez-Zacarías, Pedro;Bozdag, G. Ozan;Burnetti, Anthony;Yunker, Peter J.;Libby, Eric;Ratcliff, William C.

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所有的多细胞生物都通过两种基本途径之一发展:它们要么从自由生活的细胞聚集,创造潜在的嵌合多细胞集体,要么通过母亲-女儿细胞粘附克隆发展。虽然进化理论对这些发育模式之间的权衡做出了明确的预测,但这些模式从未在其他遗传相同的生物体中进行过实验测试。我们设计了单细胞面包酵母(酿酒酵母),使其克隆(“雪花”; Δ ace 2)或聚集(“絮状物”; GAL 1 p::FLO 1)发育,并检查了它们在波动环境中的适应性,波动环境的特征是生长期和快速沉降的选择期。当独立培养时,聚集远远上级克隆发育,在生长过程中提供35%的优势,在沉降选择过程中提供2.5倍的优势。然而,当直接竞争时,克隆发展的雪花酵母迅速取代聚集絮凝物。这是由于意想不到的社会剥削:雪花酵母,不产生粘性FLO 1,但成为融入絮凝体的频率高于絮凝体细胞本身。嵌合集群的群体比单独的絮凝物沉降得快得多,在竞争中为雪花酵母提供了适应性优势。数学模型表明,这种发展作弊可能很难规避;假设的“挑剔的絮凝物”,以避免利用维持克隆支付生态成本时,罕见的,往往导致其灭绝。我们的研究结果突出了聚集性发展的核心冲突:非特异性细胞结合提供了强大的生态优势快速形成群体的能力,但正是这一特征导致了它的利用。
All multicellular organisms develop through one of two basic routes: they either aggregate from free-living cells, creating potentially chimeric multicellular collectives, or they develop clonally via mother-daughter cellular adhesion. Although evolutionary theory makes clear predictions about trade-offs between these developmental modes, these have never been experimentally tested in otherwise genetically identical organisms. We engineered unicellular baker's yeast (Saccharomyces cerevisiae) to develop either clonally ("snowflake"; Δace2) or aggregatively ("floc"; GAL1p::FLO1) and examined their fitness in a fluctuating environment characterized by periods of growth and selection for rapid sedimentation. When cultured independently, aggregation was far superior to clonal development, providing a 35% advantage during growth and a 2.5-fold advantage during settling selection. Yet when competed directly, clonally developing snowflake yeast rapidly displaced aggregative floc. This was due to unexpected social exploitation: snowflake yeast, which do not produce adhesive FLO1, nonetheless become incorporated into flocs at a higher frequency than floc cells themselves. Populations of chimeric clusters settle much faster than floc alone, providing snowflake yeast with a fitness advantage during competition. Mathematical modeling suggests that such developmental cheating may be difficult to circumvent; hypothetical "choosy floc" that avoid exploitation by maintaining clonality pay an ecological cost when rare, often leading to their extinction. Our results highlight the conflict at the heart of aggregative development: non-specific cellular binding provides a strong ecological advantage—the ability to quickly form groups—but this very feature leads to its exploitation.
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