The Evolution of Allorecognition Specificity in Clonal Invertebrates

[9402797]同种异体识别被定义为将自己与同一物种的其他成员区分开来的能力。虽然同种异体识别曾经被认为是脊椎动物免疫系统的标志，但现在很清楚，几乎所有的外壳克隆生物都具有特异性与脊椎动物免疫系统相媲美的同种异体识别系统。越来越多的证据支持克隆生物的异体识别特异性是基于遗传的结论，相对较少的基因座控制这种特异性的表达。因此，赋予同种异体识别特异性的位点必须携带大大超过其他多态性位点特征水平的遗传变异水平。这一提议的主要目标是分析——从遗传学和生态学的角度——如此高水平的遗传变异是如何在进化中维持的。三种类型的假说被提出来解释同种异体识别特异性的进化。首先，遗传变异在功能上不重要，这是一个不可行的解释，因为我们知道突变率、种群大小和异体识别位点上核苷酸替代的模式。后两个假设援引了自然选择；它们的不同之处是，选择是直接调节组织相互作用的结果，还是通过异体识别的相关效应间接起作用，比如对交配偏好的控制。与脊椎动物相比，在脊椎动物中，持续的组织相互作用是罕见的，而在无脊椎动物中，当它们与同种竞争可居住空间时，这种接触经常发生。同种异体识别系统通过决定它们是否会导致基因型间融合、排斥或攻击来调节这种相互作用的性质和结果。定量模型证实同种异体识别特异性可以通过其对竞争相互作用结果的影响而进化。选择在多大程度上促进特异性积累的关键决定因素包括融合、排斥和排斥的成本和收益，以及相容（即融合）和不相容（即排斥或攻击性）基因型相互作用的频率。该项目将通过估算两种覆壳无脊椎动物的成本、收益和相互作用频率来评估同种异体识别特异性是如何演变的。在一个种群海鞘（Botryllus schlosseri）中，同种异体识别系统控制着同种相遇是导致融合还是排斥。在其他物种中，共生体水螅虫（Hydractinia symbiolongicarpus），同种相遇的另一种结果是融合或攻击。它还将评估一个广泛引用的多效性机制的优点，通过该机制也可以维持同种异体识别的特异性，即配子相互作用的控制。通过比较这两个物种的异型多样性是如何进化的，这项研究将为理解几乎每个物种的个体如何以及为什么能够区分自我和非自我奠定基础。

9402797 Grosberg Allorecognition is defined as the ability to distinguish self from other members of the same species. Although allorecognition was once thought to be the hallmark of the vertebrate immune system, it is now clear that virtually all encrusting clonal organisms possess allorecognition systems whose specificity rivals that of the vertebrate immune system. A growing body of evidence supports the conclusion that allorecognition specificity in clonal organisms is genetically based, and that relatively few loci control the expression of this specificity. Consequently, the loci that confer allorecognition specificity must carry levels of genetic variation that greatly exceed levels characteristic of other polymorphic loci. The major goal of this proposal is to analyze -- from both a genetical and ecological perspective -- how such extraordinarily high levels of genetic variation are evolutionarily maintained. Three types of hyporthesis have been advanced to explain the evolution of allorecognition specificity. The first, that the genetic variation is functionally unimportant, is not a viable explanation, given what is known about mutation rates, population sizes, and patterns of nucleotide substitution at allorecognition loci. The second two hypotheses invoke natural selection; they differ with respect to whether selection acts directly to regulate the outcomes of tissue interactions, or whether selection acts indirectly via a correlated effect of allorecognition, such as the control of mating preferences. In contrast to vertebrates, in which sustained tissue interactions are rare, such encounters occur frequently among clonial invertebrates as they compete with conspecies for habitable space. Allorecognition systems mediate the nature and outcomes of such interactions by dictating whether they will lead to intergenotypic fusion, rejection, or aggression. Quantitative models confirm that allorecognition specificity can evolve, through its effects on the outcomes of competitive interactions. The key determinants of how strongly selection promotes the accumulation of specificity include the costs and benefits of fusion, rejections, and rejection,and the frequencies with which compatible (i.e. fusible) and incompatible (i.e. rejecting or aggressive) genotypes interact. This project will evaluate how allorecognition specificity evolves by estimating these costs, benefits, and interaction frequencies in two species of encrusting, clonal invertebrate. In one species the colonial sea squirt Botryllus schlosseri, allorecognition systems control whether conspecific encounters lead to fusion or rejection. In the other species, the cnidarian Hydractinia symbiolongicarpus, the alternative outcomes of conspecific encounters are fusion versus aggression. It will also evaluate the merits of one widely invoked pleiotropic mechanism by which allorecognition specificity could also be maintained, namely the control of gametic interations. By comparing how allotypic diversity evolves in both species, this research will build a foundation for understanding how and why individuals of nearly every species can distinguish self from nonself.