The changing pace of insular life: 5000 years of microevolution in the Orkney vole (Microtus arvalis orcadensis)

Island evolution may be expected to involve fast initial morphological divergence followed by stasis. We tested this model using the dental phenotype of modern and ancient common voles (Microtus arvalis), introduced onto the Orkney archipelago (Scotland) from continental Europe some 5000 years ago. First, we investigated phenotypic divergence of Orkney and continental European populations and assessed climatic influences. Second, phenotypic differentiation among Orkney populations was tested against geography, time, and neutral genetic patterns. Finally, we examined evolutionary change along a time series for the Orkney Mainland. Molar gigantism and anterior-lobe hypertrophy evolved rapidly in Orkney voles following introduction, without any transitional forms detected. Founder events and adaptation appear to explain this initial rapid evolution. Idiosyncrasy in dental features among different island populations of Orkney voles is also likely the result of local founder events following Neolithic translocation around the archipelago. However, against our initial expectations, a second marked phenotypic shift occurred between the 4th and 12th centuries AD, associated with increased pastoral farming and introduction of competitors (mice and rats) and terrestrial predators (foxes and cats). These results indicate that human agency can generate a more complex pattern of morphological evolution than might be expected in island rodents.

Continental-Scale Footprint of Balancing and Positive Selection in a Small Rodent (Microtus arvalis)

Genetic adaptation to different environmental conditions is expected to lead to large differences between populations at selected loci, thus providing a signature of positive selection. Whereas balancing selection can maintain polymorphisms over long evolutionary periods and even geographic scale, thus leads to low levels of divergence between populations at selected loci. However, little is known about the relative importance of these two selective forces in shaping genomic diversity, partly due to difficulties in recognizing balancing selection in species showing low levels of differentiation. Here we address this problem by studying genomic diversity in the European common vole (Microtus arvalis) presenting high levels of differentiation between populations (average FST = 0.31). We studied 3,839 Amplified Fragment Length Polymorphism (AFLP) markers genotyped in 444 individuals from 21 populations distributed across the European continent and hence over different environmental conditions. Our statistical approach to detect markers under selection is based on a Bayesian method specifically developed for AFLP markers, which treats AFLPs as a nearly codominant marker system, and therefore has increased power to detect selection. The high number of screened populations allowed us to detect the signature of balancing selection across a large geographic area. We detected 33 markers potentially under balancing selection, hence strong evidence of stabilizing selection in 21 populations across Europe. However, our analyses identified four-times more markers (138) being under positive selection, and geographical patterns suggest that some of these markers are probably associated with alpine regions, which seem to have environmental conditions that favour adaptation. We conclude that despite favourable conditions in this study for the detection of balancing selection, this evolutionary force seems to play a relatively minor role in shaping the genomic diversity of the common vole, which is more influenced by positive selection and neutral processes like drift and demographic history.

Ignoring heterozygous sites biases phylogenomic estimates of divergence times: implications for the evolutionary history of Microtus voles

Phylogenetic reconstruction of the evolutionary history of closely related organisms may be difficult because of the presence of unsorted lineages and of a relatively high proportion of heterozygous sites that are usually not handled well by phylogenetic programs. Genomic data may provide enough fixed polymorphisms to resolve phylogenetic trees, but the diploid nature of sequence data remains analytically challenging. Here, we performed a phylogenomic reconstruction of the evolutionary history of the common vole (Microtus arvalis) with a focus on the influence of heterozygosity on the estimation of intraspecific divergence times. We used genome-wide sequence information from 15 voles distributed across the European range. We provide a novel approach to integrate heterozygous information in existing phylogenetic programs by repeated random haplotype sampling from sequences with multiple unphased heterozygous sites. We evaluated the impact of the use of full, partial, or no heterozygous information for tree reconstructions on divergence time estimates. All results consistently showed four deep and strongly supported evolutionary lineages in the vole data. These lineages undergoing divergence processes split only at the end or after the last glacial maximum based on calibration with radiocarbon-dated paleontological material. However, the incorporation of information from heterozygous sites had a significant impact on absolute and relative branch length estimations. Ignoring heterozygous information led to an overestimation of divergence times between the evolutionary lineages of M. arvalis. We conclude that the exclusion of heterozygous sites from evolutionary analyses may cause biased and misleading divergence time estimates in closely related taxa.

Tracing reinforcement through asymmetrical partner preference in the European common vole Microtus arvalis

Background The mechanistic basis of speciation and in particular the contribution of behaviour to the completion of the speciation process is often contentious. Contact zones between related taxa provide a situation where selection against hybridization might reinforce separation by behavioural mechanisms, which could ultimately fully isolate the taxa. One of the most abundant European mammals, the common vole Microtus arvalis, forms multiple natural hybrid zones where rapidly diverging evolutionary lineages meet in secondary contact. Very narrow zones of hybridization spanning only a few kilometres and sex-specific gene flow patterns indicate reduced fitness of natural hybrids and incipient speciation between some of the evolutionary lineages. In this study, we examined the contribution of behavioural mechanisms to the speciation process in these rodents by fine-mapping allopatric and parapatric populations in the hybrid zone between the Western and Central lineages and experimental testing of the partner preferences of wild, pure-bred and hybrid female common voles. Results Genetic analysis based on microsatellite markers revealed the presence of multiple parapatric and largely non-admixed populations at distances of about 10 km at the edge of the area of natural hybridization between the Western and Central lineages. Wild females from Western parapatric populations and lab-born F1 hybrids preferred males from the Western lineage whereas wild females of Central parapatric origin showed no measurable preference. Furthermore, wild and lab-born females from allopatric populations of the Western or Central lineages showed no detectable preference for males from either lineage. Conclusions The detected partner preferences are consistent with asymmetrical reinforcement of pre-mating reproductive isolation mechanisms in the European common vole and with earlier results suggesting that hybridization is more detrimental to the Western lineage. As a consequence, these differences in behaviour might contribute to a further geographical stabilization of this moving hybrid zone. Such behavioural processes could also provide a mechanistic perspective for frequently-detected asymmetrical introgression patterns in the largely allopatrically diversifying Microtus genus and other rapidly speciating rodents.

“Living on the edge” : the role of field margins for common vole (Microtus arvalis) populations in recently colonised Mediterranean farmland

Acknowledgments RRP was supported by a PhD-studentship from the University of Valladolid (co-funded by Banco Santander, RR 30/04/2014). Financial support was provided by ECOCYCLES (BIODIVERSA 2008, Era-net European project, EUI2008-03658 and NERC NE/G002045/1 to XL) and ECOVOLE projects (CGL2012-35348; Ministerio de Economía y Competitividad of Spain). The article also contributes to project ECOTULA (CGL2015-66962-C2-1-R). We held all the necessary licenses and permits for conducting this work (JJLL, FM and RRP held animal experimentation permits of level B for Spain, and a capture permit was provided by the Consejería de Fomento y Medio Ambiente, Junta de Castilla y León (Expte: EP/CYL/665/2014)). We thank two anonymous reviewers for providing and constructive comments to improve the manuscript.

Chromosomal mechanisms underlying the karyotype evolution of the oriental voles (Muridae, Eothenomys)

We have investigated the karyotype relationships of two oriental voles, i.e. the Yulong vole (Eothenomys proditor, 2n = 32) and the large oriental vole (Eothenomys miletus, 2n = 56) as well as the Clarke's vole (Microtus clarkei, 2n = 52), by a combined a

雄性柴达木根田鼠断奶后对亲本尿气味的记忆

为了研究亲子分开后雄性柴达木根田鼠（Microtus limnophylus）对亲本尿气味的记忆持续时间,分别在未分开（20日龄）,以及分开10d（30日龄）、20d（40日龄）、30d（50日龄）、40d（60日龄）时,以新鲜尿作为气味源,在行为观察箱中记录雄性柴达木根田鼠对不同气味源的行为响应模式。结果表明：（1）未分开时,雄鼠对父本气味的接近频次显著高于陌生雄鼠气味;分开10d时,雄鼠对父本气味的访问时间显著多于对陌生雄鼠气味的访问时间;分开20d时,雄鼠对陌生雄鼠气味的接近潜伏期极显著短于父本,对陌生雄鼠气味的访问时间极显著长于父本,其遭遇父鼠气味时的自我修饰频次显著少于陌生雄鼠气味。（2）分开30d后,雄鼠对父本和陌生雄鼠气味的行为响应没有明显差异。以上结果表明,在亲子分开20d时,雄鼠仍能识别父本与陌生雄鼠的气味;在分开30d后,雄鼠不再能够识别父本与陌生雄鼠的气味。（3）在未分窝时,雄性柴达木根田鼠幼仔对母本和陌生雌鼠气味的行为响应没有任何差异。（4）在分开10d时,雄性柴达木根田鼠对母本和陌生雌鼠气味表现出不同的行为响应模式;分开20～40d时,雄鼠对母本与陌生雌鼠气味的行为响应没有任何差异。以上结果表明,在亲子分开10d时,雄鼠仍能识别母本与陌生雌鼠的气味;在分开20d后,雄鼠不再能够识别母本与陌生雌鼠的气味。因此,雄鼠对父本气味的嗅觉记忆时间可以持续到亲子分开20～30d之间;其对母本气味的嗅觉记忆时间可以持续到亲子分开10d时。

人工饲养条件下根田鼠肥满度的研究

实验室条件下，利用根田鼠1～70日龄体重和体长数据，计算其肥满度指数，目的在于分析其生长发育的基本规律。结果表明，根田鼠1～70日龄肥满度存在性别差异且随日龄增加而增大；雌雄个体的发育不同步；常见曲线回归模型对根田鼠1～70日龄的肥满度不能准确拟合，根据其生长发育状况，将其划分为3个阶段（其中幼体和成体阶段各含2个阶段）。

高原鼢鼠四肢骨的进化适应性分析

通过对比分析了高寒草甸生态系统的高原鼢鼠(Myospalax baileyi)、高原鼠兔(Ochotona curzoniae)及根田鼠(Microtus oeconomus)的四肢骨,结果表明,地下啮齿动物高原鼢鼠的四肢骨比地面种类高原鼠兔和根田鼠的对应骨骼粗壮,显示其较强的挖掘能力.与挖掘效率相关的尺骨挖掘动力臂系数,高原鼢鼠为0.361 7,而高原鼠兔和根田鼠不到0.17.高原鼢鼠与其他两物种的四肢骨重量分布也明显不同:高原鼢鼠的前肢骨重量超过后肢骨,而高原鼠兔及根田鼠则正好相反;高原鼠兔及根田鼠的桡尺骨重量在四肢骨中最低,而高原鼢鼠的桡尺骨重量在四肢骨中则最高.这些特征反映了地下啮齿动物为了适应地下生活方式,其四肢骨骼系统已经发生了显著变化,这对于研究地下啮齿动物的进化适应性问题具有重要意义.

捕食和食物交互作用条件下根田鼠季节性波动种群攻击水平及其行为多态性分析

在捕食和附加食物交互作用条件下,以恐吓、进攻、追逐、争斗及回避5类行为为变量,以恐吓、进攻、追逐计数之和的平均值作为攻击水平,测定根田鼠种群不同波动时期成体的攻击水平.发现根田鼠的攻击性与种群波动时期之间,存在明显的关联.统计分析结果表明,在种群3个波动时期,4种处理种群两性攻击型个体比例差异显著.除预防捕食者无附加食物（-P,-F）种群的雌体外,其它处理种群增长期和高峰期雌性和雄性攻击型个体的比例高于其衰减期.其中,预防捕食者附加食物（-P,＋F）种群、-P,-F种群及未预防捕食者附加食物（＋P,＋F）种群,雄性攻击型个体的比例均为增长期＞高峰期＞衰减期;在未预防捕食者无附加食物（＋P,-F）种群,雄性攻击型个体比例为高峰期＞增长期＞衰减期.各处理种群雌性攻击型个体比例的格局与雄体的不同.其中,-P,＋F种群及＋P,＋F种群为增长期＞高峰期＞衰减期,＋P,-F种群为高峰期＞增长期＞衰减期,而-P,-F种群攻击型个体比例为高峰期＞衰减期＞增长期.虽不同处理种群雌体及雄体的5类行为变量与种群密度的相关性不一致,而具有明显攻击性的恐吓、进攻及争斗3类行为则分别与种群密度呈显著或极显著的线性正相关关系,其结果与Chitty多态行为假设预测的一致;验证了所提出的特定假设：种群外部因子捕食和食物交互效应介导的攻击行为选择,是引起田鼠类种群季节性波动的主要内部因子.

艾虎对不同猎物的选择性

在室内条件下,将高原鼢鼠（Myospalax baileyi）、高原鼠兔（Ochotona curzoniae）和根田鼠（Microtus oeconomus）作为艾虎（Mustela eversmanni）的猎物选择对象,研究艾虎对猎物的选择性及艾虎捕杀猎物的行为时间分配.实验结果表明：艾虎对三种猎物的搜寻时间和搜寻频次基本一致,在搜寻猎物的过程中并非已知洞道系统中所存在的食物信息,是一种机会主义的捕食者;艾虎除了具有典型鼬科动物捕杀猎物的方法外,能够根据猎物的大小、活动性和反捕食能力采用不同的捕杀方法,在捕杀猎物的过程中首先捕杀高原鼢鼠,其致死部位全部为头部,其次捕杀高原鼠兔,其致死部位除了头部外,明显增加了颈部的比例,最后捕杀根田鼠,其致死部位主要是头部和胸部;艾虎在捕杀猎物的过程中,追击根田鼠的时间最多,追击鼢鼠的时间最少,而用于捕杀根田鼠的时间最少,用于捕杀鼢鼠的时间最多,艾虎捕杀高原鼠兔后单位时间内获得的能量值最大,其次为捕杀高原鼢鼠,而捕杀根田鼠后单位时间内活动的能量值最小.因此,在室内条件下艾虎对猎物的选择性主要依赖于其本身处理猎物的行为时间分配和猎物的反捕食行为,使单位时间内获得的能量值最大[动物学报 52（3）：437-443,2006].

退耕还林还草地鼠类调查及控制对策研究

2002-2003年对青海省大通县退耕还林还草地鼠类组成进行调查研究,捕获鼠类6种728只,以根田鼠Microtus oeconomus和高原鼢鼠Myospalax baileyi为绝对优势种.4种方法进行退耕还林还草地害鼠控制的结果表明:人工置夹和药物控制是地上害鼠控制的有效方法,人工地箭与灭鼠雷可有效控制地下高原鼢鼠的数量.但从长远来看,控制退耕还林还草地鼠害应采取生态治理的原则和方法.

根田鼠对不同类型栖息地的利用

为研究根田鼠(Microtus oeconomus)对不同类型栖息地的利用强度,于2002-2003年的7-9月在中国科学院海北高寒草甸生态系统定位站地区采用样方法测定了4种类型栖息地(人工耕作地、真草甸、沼泽化草甸、金露梅灌丛)中的3个根田鼠活动强度变量(跑道长度、跑道分叉数、洞口数).除了跑道长度和跑道分叉数在真草甸和沼泽化草甸间差异不显著外,3活动强度变量在不同类型栖息地间均差异显著,而且变化趋势一致;根田鼠对4类栖息地的利用强度从大到小依次为金露梅灌丛、沼泽化草甸、真草甸、人工耕作地.整体上根田鼠表现为偏好利用食物资源丰富、没有竞争性啮齿类栖息、较为郁闭的栖息地.

Diet shift of upland buzzards (Buteo hemilasius): evidence from stable carbon isotope ratios

We measured the stable carbon isotope ratios for muscle of the upland buzzards (Buteo hemilasius), plateau pika (Ochotoma curzoniae), root vole (Microtus oeconomus), plateau zokor (Myospalax fontanierii) and passerine bird species at the Haibei Alpine Meadow Ecosystem Research Station (HAMERS), and provided diet information of upland buzzards with the measurement of stable carbon isotopes in tissues of these consumers. The results showed that δ~(13)C values of small mammals and passerine bird species ranged from -25.57‰ to -25.78‰ (n = 12), and from -24.81‰ to -22.51% (n = 43), respectively, δ~(13)C values of the upland buzzards ranged from -22.60‰ to -23.10‰ when food was not available. The difference in δ~(13)C values (2.88‰±0.31‰) between upland buzzards and small mammals was much larger than the differences reported previously, 1‰-2‰, and showed significant difference, while 1.31‰±0.34‰ between upland buzzard and passerine bird species did not differ from the previously reported trophic fractionation difference of 1‰-2‰. Estimation of trophic position indicated that upland buzzards stand at trophic position 4.23, far from that of small mammals, i.e., upland buzzards scarcely captured small mammals as food at the duration of food shortage. According to isotope mass balance model, small mammals contributed 7.89% to 35.04% of carbon to the food source of the upland buzzards, while passerine bird species contributed 64.96% to 92.11%. Upland buzzards turned to passerine bird species as food during times of shortage of small mammals. δ~(13)C value, a useful indicator of diet, indicates that the upland buzzards feed mainly on passerine bird species rather than small mammals due to "you are what you eat" when small mammal preys are becoming scarce.