Gene flow and genetic structure of two of Arkansas’s rarest darter species (Teleostei: Percidae), the Arkansas Darter, Etheostoma cragini, and the Least Darter, E. microperca

Justin S. Baker, B. Wagner, R. Wood
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Abstract

Distinguishing the effects of naturally caused historical fragmentation from those of contemporary landscape modification is critically important to understanding the consequences of human influences on patterns of gene flow and population dynamics. Nonetheless, relatively few recent studies focusing on this issue have dealt with species that showed evidence of historical fragmentation. In the current study, we disentangled the effects of fragmentation operating over separate timescales on two darter species, Etheostoma cragini and E. microperca, from the Ozark Highlands. Formerly more wide-spread within this region in Arkansas, these species now occur only in highly isolated habitats (i.e., spring-runs). We separated fragmentation effects at distinct spatial and temporal scales by using several molecular loci (i.e., mtDNA/nuclear DNA/nuclear microsatellite DNA), as well as a variety of analytical approaches. Sequence divergence among Ozark and northern populations of E. microperca indicate long-standing isolation resulting from vicariant events. Both species were further isolated in unique ‘island’ habitats, sometimes at fine spatial scales, as shown by sequence divergence among Ozark Highland populations of E. cragini. Microsatellite data also revealed additional subdivision among Arkansas populations with E. cragini divided into three distinct populations and E. microperca into two. Overall, migration rates were similar among contemporary and historical time periods although patterns of asymmetric migration were inverted for E. cragini. Estimates of contemporary effective population size (Ne) were substantially lower for both species than past population sizes. Overall, historical processes involving natural fragmentation have had long-lasting effects on these species, potentially making them more susceptible to current anthropogenic impacts. Introduction Habitat fragmentation operating both over historical time scales and over more recent timescales results in species with highly fragmented distributions, significantly compromising the maintenance of genetic diversity and population viability (Keyghobadi et al. 2005; Zellmer and Knowles 2009). Distinguishing between these time scales is important to conservation efforts because knowledge of historical population structure is essential to assessing the impact of current anthropogenic effects. Several recent studies comparing past and current patterns of gene flow among populations have revealed that recent human activities have substantially altered connectivity among populations, resulting in increased bottlenecks and high levels of inbreeding (Reed et al. 2011; Apodaca et al. 2012; Blakney et al. 2014); others suggest the high levels of structure observed among populations reflect long-standing limited dispersal of the species rather than recent habitat fragmentation (Chiucchi and Gibbs, 2010). These two causes of fragmentation may also act synergistically, such that the historically fragmented populations of a species become reduced in number or each experience declines in membership due to anthropogenic effects. Populations that are both highly fragmented and exhibit reduced population sizes have high rates of local extinction and therefore higher probability of global extinction (Templeton et al. 1990). Recent fragmentation may also substantially influence metapopulation dynamics, which may play a critical role in contributing to adaptive differences observed among populations even at small spatial scales (Zellmer
两个阿肯色州的基因流和遗传结构™s最稀有的镖鲈物种(Teleostei:珀科),阿肯色州镖鲈,Etheostoma cragini,和最小镖鲈E.microperca
区分自然造成的历史碎片化和当代景观改造的影响,对于理解人类影响对基因流动模式和人口动态的影响至关重要。尽管如此,最近关注这一问题的研究相对较少涉及显示出历史碎片证据的物种。在目前的研究中,我们解开了在不同时间尺度上碎片化对Ozark高地的两种飞镖物种,Etheostoma cragini和E.microperca的影响。这些物种以前在阿肯色州的这一地区分布更广,现在只出现在高度孤立的栖息地(即春季迁徙)。我们通过使用几个分子位点(即mtDNA/核DNA/核微卫星DNA)以及各种分析方法,在不同的空间和时间尺度上分离了碎片效应。Ozark和北部种群的微小锥虫序列差异表明,替代事件导致了长期的孤立。这两个物种都在独特的“岛屿”栖息地被进一步隔离,有时是在精细的空间尺度上,正如克拉基尼的奥扎克高地种群之间的序列差异所示。微卫星数据还揭示了阿肯色州种群的进一步细分,cragini E.cragini被分为三个不同的种群,microperca E.被分为两个。总体而言,当代和历史时期的移民率相似,尽管克拉基尼的非对称移民模式相反。对这两个物种的当代有效种群规模(Ne)的估计大大低于过去的种群规模。总的来说,涉及自然破碎化的历史过程对这些物种产生了长期影响,可能使它们更容易受到当前人类活动的影响。引言栖息地在历史时间尺度和最近时间尺度上的碎片化导致物种分布高度碎片化,严重影响遗传多样性和种群生存能力的维持(Keyghobadi等人,2005;Zellmer和Knowles,2009年)。区分这些时间尺度对保护工作很重要,因为了解历史种群结构对于评估当前人为影响的影响至关重要。最近几项比较过去和现在种群之间基因流动模式的研究表明,最近的人类活动大大改变了种群之间的连通性,导致瓶颈增加和近亲繁殖率高(Reed等人,2011;Apodaca等人2012;Blakney等人2014);其他人认为,在种群中观察到的高水平结构反映了该物种长期有限的扩散,而不是最近的栖息地破碎化(Chiucchi和Gibbs,2010)。这两个碎片化的原因也可能协同作用,使得一个物种历史上碎片化的种群数量减少,或者由于人为影响,每个种群的成员数量都有所减少。高度分散和种群规模缩小的种群局部灭绝率很高,因此全球灭绝的可能性更高(Templeton等人,1990)。最近的碎片化也可能对集合种群的动力学产生重大影响,即使在小的空间尺度上,集合种群的动态也可能在种群之间观察到的适应性差异中发挥关键作用(Zellmer
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