Mechanisms for polyandry evolution in a complex social bee

IF 1.9 2区生物学 Q3 BEHAVIORAL SCIENCES Behavioral Ecology and Sociobiology Pub Date : 2024-03-09 DOI:10.1007/s00265-024-03450-x

Keith Delaplane, Katherine Hagan, Kevin Vogel, Lewis Bartlett

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Abstract

Polyandry in social Hymenoptera is associated with reduced within-colony relatedness and increased colony-level ecologic fitness. One explanation for this sees increasing within-nest genetic diversity as a mechanism for improving group task efficiency and colony competitiveness. A queen on her mating flight captures nearly 90% of her breeding population’s allele potential by her tenth effective mating (m_e ~ 10 males). Under this population allele capture (PAC) model, colony fitness gains track mating number in an asymptotic manner, leveling out after about the tenth mating. A supporting theory we call the genotype composition (GC) model sees genetic novelty at mating levels higher than the m_e ~ 10 asymptote, the hyperpolyandry zone, resulting from unique genotype compositions whose number are potentially infinite. Colony fitness gains under the GC model will track mating number in a linear manner. We set up field colonies with Apis mellifera queens each instrumentally mated with 1, 2, 4, 8, 16, or 32 males, creating a polyandry gradient bracketing the qualitative divide of m_e ~ 10, measured tokens of colony level fitness, and collected observation hive data. Our results lead us to conclude that (1) ancestral colony traits fundamental to eusociality (cooperative brood care) respond to mating level changes at or below m_e ~ 10 in a manner consistent with the PAC model, whereas (2) more derived specialized colony phenotypes (resistance to the non-native parasite Varroa destructor) continue improving with increasing m_e in a manner consistent with the GC model. By either model, (3) the mechanism for increasing colony fitness is an increase in worker task specialisms and task efficiency.

Significance statement

Polyandry is a female’s practice of mating with many males, storing their sperm, and using it to produce genetically diverse offspring. In complex social bees, a queen captures nearly 90% of her breeding population’s diversity potential by her tenth mating; however, queens in nature routinely mate with many more than ten males. We tested two models that, together, explain how social bee colonies ecologically benefit from queen mating numbers ranging from 2 to potential infinity. A population allele capture (PAC) model focuses on colony fitness gains at mating numbers at or below 10, and we provide evidence that it was at these polyandry levels that significant gains were made in an ancestral eusocial trait, cooperative brood care. A genotype composition (GC) model focuses on colony fitness gains at higher mating numbers, and we believe these gains are centered around more recently evolved ecologic specialisms such as parasite resistance.

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复杂社会性蜜蜂的多雄性进化机制

摘要社会性膜翅目昆虫的多雄性与群内亲缘关系的降低和群级生态适应性的提高有关。对此的一种解释是，增加巢内遗传多样性是提高群体任务效率和群落竞争力的一种机制。一只蜂后在其第十次有效交配（我 ~ 10 只雄蜂）之前，会捕获其繁殖种群近 90% 的等位基因潜力。在这一群体等位基因捕获（PAC）模型下，蜂群适应性的提高以渐进的方式跟踪交配次数，大约在第十次交配后趋于平稳。我们称之为基因型组成（GC）模型的支持理论认为，在交配水平高于 me ~ 10 的渐近线（即超多雄区）时，遗传新颖性来自于独特的基因型组成，其数量可能是无限的。在 GC 模型下，蜂群的适应性收益将以线性方式跟踪交配数量。我们在野外建立了蜂群，每只蜂王分别与 1、2、4、8、16 或 32 只雄蜂进行工具交配，形成了 "我"~"10 "定性分界线范围内的多雄性梯度，测量了蜂群水平的适应性标记，并收集了观察蜂巢的数据。我们的研究结果使我们得出以下结论：(1)蜂群的祖先性状（合作育雏）对 me ~ 10 或更低的交配水平变化的反应与 PAC 模式一致，而(2)更多衍生的专门化蜂群表型（对非本地寄生虫破坏者 Varroa 的抵抗力）随着 me 的增加而继续改善，其方式与 GC 模式一致。无论采用哪种模式，(3) 提高蜂群适合度的机制都是提高工蜂的任务专业性和任务效率。重要意义声明多配偶制是雌蜂与许多雄蜂交配，储存雄蜂的精子，并利用这些精子培育出基因多样化的后代。在复杂的社会性蜜蜂中，蜂王在第十次交配时可获得其繁殖种群近 90% 的多样性潜力；然而，自然界中的蜂王通常会与十多只雄蜂交配。我们对两个模型进行了测试，这两个模型共同解释了社会蜂群如何从蜂王交配数量（从 2 到潜在的无穷大）中获得生态效益。种群等位基因捕获（PAC）模型侧重于交配数为 10 或低于 10 时蜂群的适应性收益，我们提供的证据表明，正是在这些多育水平上，祖先的社会性特征--合作育雏--获得了显著收益。基因型组成（GC）模型的重点是交配数较高时的蜂群适应性收益，我们认为这些收益主要集中在最近进化出的生态特异性上，如寄生虫抵抗力。

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来源期刊

Behavioral Ecology and Sociobiology 生物-动物学

CiteScore

3.90

自引率

8.70%

发文量

146

审稿时长

3 months

期刊介绍： The journal publishes reviews, original contributions and commentaries dealing with quantitative empirical and theoretical studies in the analysis of animal behavior at the level of the individual, group, population, community, and species.