Hurst Gregory D D
Institute of Integrative Biology, University of Liverpool, Liverpool L69 7ZB, UK.
Interface Focus. 2017 Oct 6;7(5):20170001. doi: 10.1098/rsfs.2017.0001. Epub 2017 Aug 18.
Many aspects of an individual's biology derive from its interaction with symbiotic microbes, which further define many aspects of the ecology and evolution of the host species. The centrality of microbes in the function of individual organisms has given rise to the concept of the holobiont-that an individual's biology is best understood as a composite of the 'host organism' and symbionts within. This concept has been further elaborated to posit the holobiont as a unit of selection. In this review, I critically examine whether it is useful to consider holobionts as a unit of selection. I argue that microbial heredity-the direct passage of microbes from parent to offspring-is a key factor determining the degree to which the holobiont can usefully be considered a level of selection. Where direct vertical transmission (VT) is common, microbes form part of extended genomes whose dynamics can be modelled with simple population genetics, but that nevertheless have subtle quantitative distinctions from the classic mutation/selection model for nuclear genes. Without direct VT, the correlation between microbial fitness and host individual fitness erodes, and microbe fitness becomes associated with host survival only (rather than reproduction). Furthermore, turnover of microbes within a host may lessen associations between microbial fitness with host survival, and in polymicrobial communities, microbial fitness may derive largely from the ability to outcompete other microbes, to avoid host immune clearance and to minimize mortality through phage infection. These competing selection pressures make holobiont fitness a very minor consideration in determining symbiont evolution. Nevertheless, the importance of non-heritable microbes in organismal function is undoubted-and as such the evolutionary and ecological processes giving rise to variation and evolution of the microbes within and between host individuals represent a key research area in biology.
个体生物学的许多方面源于其与共生微生物的相互作用，而这进一步界定了宿主物种生态和进化的诸多方面。微生物在个体生物功能中的核心地位催生了全生物的概念——即个体生物学最好被理解为“宿主生物体”与其内共生体的复合体。这一概念已得到进一步阐述，将全生物假定为一个选择单位。在本综述中，我批判性地审视将全生物视为一个选择单位是否有用。我认为微生物遗传——微生物从亲代直接传递给子代——是决定全生物在多大程度上可被有效视为一个选择层面的关键因素。在直接垂直传播（VT）常见的情况下，微生物构成扩展基因组的一部分，其动态可用简单的群体遗传学来建模，但与核基因的经典突变/选择模型仍存在细微的数量差异。没有直接的VT，微生物适应性与宿主个体适应性之间的相关性就会减弱，微生物适应性仅与宿主生存相关（而非繁殖）。此外，宿主体内微生物的更替可能会减少微生物适应性与宿主生存之间的关联，在多微生物群落中，微生物适应性可能很大程度上源于在与其他微生物竞争中胜出、避免被宿主免疫清除以及将噬菌体感染导致的死亡率降至最低的能力。这些相互竞争的选择压力使得全生物适应性在决定共生体进化时成为一个非常次要的考虑因素。然而，不可遗传的微生物在生物体功能中的重要性是毋庸置疑的——因此，导致宿主个体内部和之间微生物变异与进化的进化和生态过程是生物学中的一个关键研究领域。
