Phenotypic noise and the cost of complexity

Experimental studies demonstrate the existence of phenotypic diversity despite constant genotype and environment. Theoretical models based on a single phenotypic character predict that during an adaptation event, phenotypic noise should be positively selected far from the fitness optimum because it increases the fitness of the genotype, and then be selected against when the population reaches the optimum. It is suggested that because of this fitness gain, phenotypic noise should promote adaptive evolution. However, it is unclear how the selective advantage of phenotypic noise is linked to the rate of evolution, and whether any advantage would hold for more realistic, multidimensional phenotypes. Indeed, complex organisms suffer a cost of complexity, where beneficial mutations become rarer as the number of phenotypic characters increases. Using a quantitative genetics approach, we first show that for a one-dimensional phenotype, phenotypic noise promotes adaptive evolution on plateaus of positive fitness, independently from the direct selective advantage on fitness. Second, we show that for multidimensional phenotypes, phenotypic noise evolves to a low-dimensional configuration, with elevated noise in the direction of the fitness optimum. Such a dimensionality reduction of the phenotypic noise promotes adaptive evolution and numerical simulations show that it reduces the cost of complexity.     

The timescale of environmental fluctuations determines the competitive advantages of phenotypic plasticity and rapid evolution

Organisms can respond to fluctuating environments by phenotypic plasticity and rapid evolution, both occurring on similar timescales to the environmental fluctuations. Because each adaptation mechanism has been independently studied, the effects of different adaptation mechanisms on ecological dynamics are not well understood. Here, using mathematical modeling, we compared the advantages of phenotypic plasticity and rapid evolution under conditions where the environment fluctuated between two states on various timescales. The results indicate that the advantages of phenotypic plasticity under environmental fluctuations on different timescales depend on the cost and the speed of plasticity. Both the speed of plastic adaptation and the cost of plasticity affect competition results, while the quantitative effects of them vary depending on the timescales. When the environment fluctuates on short timescales, the two populations with evolution and plasticity coexist, although the population with evolution is dominant. On moderate timescales, the two populations also coexist; however, the population with plasticity becomes dominant. On long timescales, whether the population with phenotypic plasticity or evolution is more advantageous depended on the cost of plasticity. Moreover, our results indicate that the mechanisms resulting in the dominance of the plastic population over the population with evolution are different depending on the timescales of environmental fluctuations. Therefore, the timescales of environmental fluctuations deserve more attention if we are to better understand the detailed competition results underlying phenotypic variation.     

Adaptive evolution of metabolic pathways in Drosophila

The adaptive significance of enzyme variation has been of central interest in population genetics. Yet, how natural selection operates on enzymes in the larger context of biochemical pathways has not been broadly explored. A basic expectation is that natural selection on metabolic phenotypes will target enzymes that control metabolic flux, but how adaptive variation is distributed among enzymes in metabolic networks is poorly understood. Here, we use population genetic methods to identify enzymes responding to adaptive selection in the pathways of central metabolism in Drosophila melanogaster and Drosophila simulans. We report polymorphism and divergence data for 17 genes that encode enzymes of 5 metabolic pathways that converge at glucose-6-phosphate (G6P). Deviations from neutral expectations were observed at five loci. Of the 10 genes that encode the enzymes of glycolysis, only aldolase (Ald) deviated from neutrality. The other 4 genes that were inconsistent with neutral evolution (glucose-6-phosphate dehydrogenase [G6pd]), phosphoglucomutase [Pgm], trehalose-6-phosphate synthetase [Tps1], and glucose-6phosphatase [G6pase] encode G6P branch point enzymes that catalyze reactions at the entry point to the pentose-phosphate, glycogenic, trehalose synthesis, and gluconeogenic pathways. We reconcile these results with population genetics theory and existing arguments on metabolic regulation and propose that the incidence of adaptive selection in this system is related to the distribution of flux control. The data suggest that adaptive evolution of G6P branch point enzymes may have special significance in metabolic adaptation.     

Phenotypic plasticity in gene expression contributes to divergence of locally adapted populations of Fundulus heteroclitus

We examine the interaction between phenotypic plasticity and evolutionary adaptation using muscle gene expression levels among populations of the fish Fundulus heteroclitus acclimated to three temperatures. Our analysis reveals shared patterns of phenotypic plasticity due to thermal acclimation as well as non‐neutral patterns of variation among populations adapted to different thermal environments. For the majority of significant differences in gene expression levels, phenotypic plasticity and adaptation operate on different suites of genes. The subset of genes that demonstrate both adaptive differences and phenotypic plasticity, however, exhibit countergradient variation of expression. Thus, expression differences among populations counteract environmental effects, reducing the phenotypic differentiation between populations. Finally, gene‐by‐environment interactions among genes with non‐neutral patterns of expression suggest that the penetrance of adaptive variation depends on the environmental conditions experienced by the individual.     

湖南白檀居群形态多样性及与环境的相关性

为了解白檀在湖南地区不同环境的适应性及遗传变化程度,对湖南地区6个白檀天然居群的189个个体的11个表型性状进行形态遗传多样性分析。结果表明,11个表型性状均具有丰富的遗传多样性(H'=1.389),居群间的平均方差分量为52.60%,居群内的平均方差分量为37.03%,说明在白檀形态性状多样性分布上是居群间多样性程度大于居群内,即居群间的形态变异是白檀形态变异的主要来源。聚类分析结果表明,6个居群的表型性状并没有严格依地理距离聚类,主成分与相关分析结果显示在11个表型中树型因子是主要形态变异因子,年降雨量与树型因子呈显著正相关,其他表型变异受遗传的影响可能大于受环境的影响。     

山苍子天然种群叶片和种实性状的表型多样性

为揭示山苍子(Litsea cubeba)天然种群叶片和种实性状的表型变异程度及其变异规律,调查了长江以南7个省份共10个天然种群的叶片和种实性状,并对其多样性进行分析。结果表明:1)山苍子的叶片和种实性状在种群间和种群内存在极其丰富的多样性,各性状表型分化系数(Vst)均值为60.19%,种群表型性状分化以种群间变异为主;2)果实形态、叶片形态、果实重和种子重4类性状的Vst均值分别为51.27%、66.66%、54.57%和72.29%;平均变异系数(CV)分别为6.60%、16.91%、19.71%和13.40%;果实形态的表型分化系数和变异系数最小,表明其性状最为稳定;3)10个表型性状间多数呈显著或极显著相关,性状与地理气候因子的相关性较差;4)系统聚类将10个种群共分为4类,种群间的分类并没有依地理距离而聚类,表型性状的Mahalanobis距离与地理距离的相关不显著(r=0.042,P=0.821),进一步表明山苍子叶片和种实性状的变异在空间上是不连续性的。研究结果为今后山苍子种质资源的保存和育种策略的制定奠定基础。     

Evolution of chinook salmon (Oncorhynchus tshawytscha) populations in New Zealand: pattern,rate, and process

Chinook salmon, Oncorhynchus tshawytscha, from the Sacramento River, California, USA were introduced to New Zealand between 1901 and 1907, and colonized most of their present-day range within about 10 years. The New Zealand populations now vary in phenotypic traits typically used to differentiate salmon populations within their natural range: growth in freshwater and at sea, age at maturity, dates of return to fresh water and reproduction, morphology, and reproductive allocation. This paper reviews a large research program designed to determine the relative contributions of phenotypic plasticity and genetic adaptation to this variation, in an effort to understand the processes underlying the natural evolution of new populations. We found strong evidence of trait divergence between populations within at most 30 generations, particularly in freshwater growth rate, date of return, and reproductive output, with plausible adaptive bases for these differences. Importantly, we also demonstrated not only a genetic basis for post-release survival but higher survival, and hence fitness, of a population released from its established site compared to another population released from the same site. We conclude that divergence of salmon in different rivers probably resulted initially from phenotypic plasticity (e.g., habitat-specific growth rates, and effects of upriver migration on ovarian investment). Philopatry (homing to natal streams) combined with rapid evolution of distinct breeding periods to restrict gene flow, facilitating divergence in other traits. We also suggest that in addition to genetic divergence resulting from random founder effects, divergence may also arise during the very early stages of colonization when the original colonists are a non-random, pre-adapted subset of the source population. This favored founders effect immediately improves the fitness of the new population. Overall, this research reveals the complex interplay of environmental and genetic controls over behavior, physiology and life history that characterize the early stages of population differentiation, a process that has taken place repeatedly during the history of salmon populations.     

秦巴山区野百合表型多样性

为揭示秦巴山区野百合天然居群的表型变异,对该地区17个野百合天然居群花、叶的8个质量性状和21个数量性状进行了观测。结果表明：野百合在秦巴山区适应性强、分布范围广,而且大多生长在海拔705~1913 m 的高山;表型性状变异丰富;上部叶片长与纬度存在显著正相关,柱头宽、上部叶片长与海拔高度存在显著正相关,下部叶间距与年降水量存在显著正相关,花梗长和上部叶片长与年均温度存在显著负相关;17个野百合天然居群被系统聚类为巴山和秦岭2大组。该研究结果为进一步开展野百合遗传育种、保护生物学的研究奠定了基础。     

青钱柳天然群体种子性状表型多样性

以青钱柳分布区内的9个天然群体种子为试材,对种子千粒重、体积、直径、厚度和径厚比5个表型性状进行了系统的比较分析,采用方差分析、相关分析及聚类分析等方法对群体间和群体内的表型多样性进行探讨.结果表明: 青钱柳种子千粒重、体积、直径及厚度在群体间和群体内均达到显著或极显著差异,而种子径厚比仅在群体内存在极显著差异,说明青钱柳种子性状在2个层次上都具有丰富的多样性.各性状的平均表型分化系数（V）为20.54%,即群体间的变异远低于群体内的变异（79.46%）.种子性状与地理因子相关程度存在差别,且受年均气温的影响最大.利用群体间欧氏距离进行系统聚类分析,青钱柳群体可以划分为三类.     

UNVEILing connections between genotype,phenotype, and fitness in natural populations

Understanding the links between genetic variation and fitness in natural populations is a central goal of evolutionary genetics. This monumental task spans the fields of classical and molecular genetics, population genetics, biochemistry, physiology, developmental biology, and ecology. Advances to our molecular and developmental toolkits are facilitating integrative approaches across these traditionally separate fields, providing a more complete picture of the genotype‐phenotype map in natural and non‐model systems. Here, we summarize research presented at the first annual symposium of the UNVEIL Network, an NSF‐funded collaboration between the University of Montana and the University of Nebraska, Lincoln, which took place from the 1st to the 3rd of June, 2018. We discuss how this body of work advances basic evolutionary science, what it implies for our ability to predict evolutionary change, and how it might inform novel conservation strategies.     

Evolution of adaptive phenotypic traits without positive Darwinian selection

Recent evidence suggests the frequent occurrence of a simple non-Darwinian (but non-Lamarckian) model for the evolution of adaptive phenotypic traits, here entitled the plasticity-relaxation-mutation (PRM) mechanism. This mechanism involves ancestral phenotypic plasticity followed by specialization in one alternative environment and thus the permanent expression of one alternative phenotype. Once this specialization occurs, purifying selection on the molecular basis of other phenotypes is relaxed. Finally, mutations that permanently eliminate the pathways leading to alternative phenotypes can be fixed by genetic drift. Although the generality of the PRM mechanism is at present unknown, I discuss evidence for its widespread occurrence, including the prevalence of exaptations in evolution, evidence that phenotypic plasticity has preceded adaptation in a number of taxa and evidence that adaptive traits have resulted from loss of alternative developmental pathways. The PRM mechanism can easily explain cases of explosive adaptive radiation, as well as recently reported cases of apparent adaptive evolution over ecological time.     

山荆子腊叶标本表型性状变异分析

为了揭示山荆子表型性状的变异程度和规律,以150份山荆子腊叶标本为材料,选择20个表型性状,统计基本参数并进行聚类分析.结果表明:叶的平均变异系数(CV=32.67%)大于果的平均变异系数(CV=20.7%),果的性状稳定性较高,叶性状中叶柄长变异系数(CV=38%)最大,叶宽位/叶长变异系数(CV=13.29%)最小;果实性状中果径宽位/果柄长(CV=29.37%)变异最大,变异最小的性状是果长/果径(CV=13.10%);选用平均欧氏距离对各地方居群的20个表型性状进行UPGMA聚类,在距离5阈值处,可以划分为5类,在欧氏距离6阈值处,可划分为3大类.     

云南滇龙胆居群表型多样性及其与环境关系研究

为揭示滇龙胆天然居群表型变异程度和变异规律,以云南省5个区域天然分布的20个野生居群400个单株20个表型性状指标为调查研究对象,并用变异系数、Shannon-Weiner多样性指数和巢式方差分析对滇龙胆居群间和居群内的表型变异进行分析,用相关性分析对滇龙胆表型性状与地理气象因子间的变异格局进行分析,用类平均聚类法对20个滇龙胆居群进行分类.结果表明:5个区域的滇龙胆以楚雄地区变异最大,变异系数为39.8%,变异最小的是昆明地区,为31.4%;不同居群的20个表型性状变异程度差异明显,变异系数在14.4%～91.8%之间,平均为40.4%,20个居群的平均变异为26.8%～37.0%;滇龙胆地理居群的表型分化较高,20个性状居群间的分化系数平均为73.14%,变化范围为36.03%～91.94%,居群间变异高于居群内;滇龙胆20个表型性状的总的多样性指数平均为2.547,5个不同分布区域多样性指数存在差异,最大为楚雄(1.271 4),最小为玉溪(1.266 7);表型性状变异受经度和降雨量影响较大,与纬度、海拔和温度相关性不显著;通过UPGMA聚类,滇龙胆被分成3个组,性状的表型特征并没有依地理距离而聚类....     

A natural heating experiment: Phenotypic and genotypic responses of plant phenology to geothermal soil warming

Under global warming, the survival of many populations of sedentary organisms in seasonal environments will largely depend on their ability to cope with warming in situ by means of phenotypic plasticity or adaptive evolution. This is particularly true in high‐latitude environments, where current growing seasons are short, and expected temperature increases large. In such short‐growing season environments, the timing of growth and reproduction is critical to survival. Here, we use the unique setting provided by a natural geothermal soil warming gradient (Hengill geothermal area, Iceland) to study the response of Cerastium fontanum flowering phenology to temperature. We hypothesized that trait expression and phenotypic selection on flowering phenology are related to soil temperature, and tested the hypothesis that temperature‐driven differences in selection on phenology have resulted in genetic differentiation using a common garden experiment. In the field, phenology was related to soil temperature, with plants in warmer microsites flowering earlier than plants at colder microsites. In the common garden, plants responded to spring warming in a counter‐gradient fashion; plants originating from warmer microsites flowered relatively later than those originating from colder microsites. A likely explanation for this pattern is that plants from colder microsites have been selected to compensate for the shorter growing season by starting development at lower temperatures. However, in our study we did not find evidence of variation in phenotypic selection on phenology in relation to temperature, but selection consistently favoured early flowering. Our results show that soil temperature influences trait expression and suggest the existence of genetically based variation in flowering phenology leading to counter‐gradient local adaptation along a gradient of soil temperatures. An important implication of our results is that observed phenotypic responses of phenology to global warming might often be a combination of short‐term plastic responses and long‐term evolutionary responses, acting in different directions.     

Biodiversity of Pinus (Pinaceae) in Mexico: speciation and palaeo-endemism

Mexico, with 43 species of Pinus recognized in the most recent revision for Flora Neotropica, is the richest centre of diversity for the genus. Other centres are California and south-east U.S.A. In comparison, Eurasian pine regions are less diverse. This biogeography, combined with the virtual absence of fossil evidence in Mexico, has led to the consensus that Pinus is a relative newcomer to the region and that 'recent' speciation accounts for its diversity. Phylogenetic analysis indicates that several of the oldest and most primitive members of the genus may have originated in this part of the continent and coexist with the species resulting from more recent radiation.     

Decay of unused characters by selection and drift

The reduction and loss of redundant phenotypic characters is a common feature of evolution. However, the mechanisms that drive deterioration of unused characters remain unclear. Here, we outline a simple framework where the relative importance of selective and neutral processes varies with environmental factors, because of variation in the fitness costs associated with unused traits. We tested our hypotheses using experimental evolution of the bacterium Pseudomonas fluorescens in spatially uniform environments. Results show that an unused character, swimming motility, decayed over evolutionary time and the rate of this decay varied among selection environments with different levels of resource availability. This is explained in the context of an environment-specific genetic correlation between motility and fitness, which is negative when resources are limited but neutral at higher resource levels. Thus, selection against an unused character was most effective in environments where the fitness cost was the greatest. This suggests that the same character can decay by different mechanisms depending upon environmental factors and supports previous evidence to show that resource availability can critically affect the outcomes of evolution.