Evolution on ecological timescales: a role for non-genetic inheritance in adapting to novel anthropogenic stressors?

越来越多的研究正在证明“当代进化”，即种群进化非常迅速，有时不到10代。当代的进化往往与人类活动有关，例如细菌对抗生素的耐药性、植物对金属污染的耐受性、对杀虫剂和除草剂的耐药性以及鱼类种群因过度捕捞而发生的变化。了解种群如何适应快速和持续的人为变化是预测种群持久性极限和降低物种灭绝率的必要条件。我们对进化的传统观点认为，适应是通过后代从父母那里继承基因来提高他们在当前环境中的生存和繁殖（适应性）而发生的。遗传变异被认为是由随机的基因突变产生的。但是，由于大多数随机突变降低了生物体的适应性，甚至增加适应性的随机突变最初也只发生在单个个体中，而这些个体可能无法偶然繁殖，因此很难看出单凭随机突变如何解释当代进化对快速人为变化的反应。如果种群足够大，种群中可能已经存在一种有利的突变，可以“拯救”它免于灭绝。然而，本研究将关注的一个新兴的替代假设是，种群最初是通过非基因遗传过程进化的，在这个过程中，新的表型是由DNA序列以外的因素传递产生的。当父母以不同的方式分配非遗传物质给他们的后代，改变他们的行为、形态或生理时，就会产生“亲代效应”。例如，在许多物种中，当雌性经历恶劣的环境时，它们产生的更大的后代更少。另外，当负责改变细胞中DNA折叠方式的表观遗传标记从一代遗传到下一代时，就会发生“表观遗传”，从而改变在任何给定时间开启或关闭的基因模式。从本质上讲，这与解释我们身体中不同类型的细胞如何从一次细胞分裂到下一次细胞分裂的机制是相同的。目前，我们对非基因遗传在使种群进化以应对快速环境变化方面的重要性知之甚少，也不知道可能涉及哪种机制。这是因为在有性繁殖的生物体中，每个个体都有自己独特的一套基因，这使得很难将遗传遗传与非遗传遗传分开，其次，因为非遗传遗传的研究必须进行至少3代，这在许多研究系统中是不可行的。在本研究中，我们将通过研究水蚤（Daphnia pulex）的非基因遗传来克服这些问题；繁殖周期为10天的一种生物，并进行无性繁殖，这意味着所有的后代在基因上都与它们的母亲相同。我们将通过比较基因相同的后代的生长、生存、繁殖和基因表达模式，量化暴露于不同常见淡水污染物所产生的非基因遗传。亲代效应和表观遗传的相对重要性将通过确定暴露和非暴露谱系中后代特征的差异是否可以通过后代供应的差异或基因开关模式的变化以及细胞中负责折叠DNA分子的表观遗传标记来解释。最后，我们将通过确定祖先暴露于污染物是否会改变复制基因相同群体之间竞争实验的结果来评估非基因遗传的进化意义。

Increasing numbers of studies are now demonstrating 'contemporary evolution' in which populations evolve very quickly, sometimes in less than 10 generations. Frequently, contemporary evolution is associated with human activities for example antibiotic resistance in bacteria, metal pollution tolerance in plants, pesticide and herbicide resistance, and changes in fish stocks in response to over-fishing. Understanding how populations adapt to rapid and sustained anthropogenic change is imperative for predicting limits to population persistence, and reducing species extinction rates.Our traditional view of evolution suggests that adaptation occurs through offspring inheriting genes from their parents that increase their survival and reproduction (fitness) in the current environment. Genetic variation is assumed to arise through random genetic mutations. But since most random mutations decrease an organism's fitness, and even random mutations that increase fitness initially only occur in a single individual, which might fail to breed just by chance, it is hard to see how random mutations alone can explain contemporary evolution in response to rapid anthropogenic change. If populations are large enough, an advantageous mutation may already exist in the population that can 'rescue' it from extinction. However, an emerging alternative hypothesis that this study will focus on is that populations initially evolve through a process of non-genetic inheritance, in which novel phenotypes are generated by the transmission of factors other than DNA sequence. 'Parental effects' arise when parents differentially allocate non-genetic materials to their offspring altering their behaviour, morphology, or physiology. For example, in many species females produce fewer larger offspring when they experience harsh conditions. Alternatively, 'Epigenetic inheritance' occurs when the epigenetic marks responsible for changing the way that DNA is folded in a cell is inherited from one generation to the next, changing the pattern of genes that are switched on or off at any given time. This is essentially the same mechanism that explains how distinct cell types in our bodies are maintained from one cell division to the next.Currently we have little idea how important non-genetic inheritance is in enabling populations to evolve in response to rapid environmental change, or which mechanism(s) might be involved. This is because in sexually reproducing organisms each individual has its own unique set of genes making it difficult to separate genetic inheritance from non-genetic inheritance and secondly because studies of non-genetic inheritance must be conducted over at least 3 generations, something which is not feasible in many study systems. In this study we will overcome these problems by studying non-genetic inheritance in the water flea, Daphnia pulex; an organism that has a generation time of 10 days and reproduces clonally, meaning that all offspring are genetically identical to their mothers.We will quantify the non-genetic inheritance generated by exposure to different common freshwater pollutants by comparing the growth, survival, reproduction and patterns of gene expression of genetically identical offspring from ancestors exposed to pollution or not. The relative importance of parental effects and epigenetic inheritance will be assessed by determining whether differences in offspring traits in exposed and non-exposed lineages are explained by differences in offspring provisioning or changes in the patterns of genes switched on or off and the epigenetic marks responsible for folding DNA molecules in the cell. Finally, we will assess the evolutionary implications of non-genetic inheritance by determining whether the exposure of ancestors to pollutants changes the outcome of competition experiments between replicated genetically identical populations.