Rise and fall of a hybrid zone: implications for the roles of aggression, mate choice, and secondary succession

Hybridization can be an important evolutionary force by generating new species and influencing evolution of parental species in multiple ways, including introgression and the consequences of hybrid vigor. Determining the ecological processes underlying evolution in hybrid zones is difficult however because it requires examining changes in both genotypic frequencies over time and corresponding ecological information, data that are rarely collected together. Here, we describe genetic and ecological aspects of a hybrid zone between the Eastern Fence Lizard, Sceloporus undulatus, and the Florida Scrub Lizard, Sceloporus woodi, occurring over at least 23 generations. The hybrid zone, discovered greater than 35 years ago using morphological characters, originally consisted of nearly even proportions of parental species and hybrids. Now, using genetic markers (species-diagnostic mtDNA sites and 6 nDNA microsatellite loci across a total of n = 117 individuals), we confirm not only that hybridization occurred but also that subsequent backcrossing has resulted in highly introgressed hybrids, with many hybrids containing mitochondrial DNA from one species on a nuclear DNA background of the other. Ecological aspects explaining these shifts in genetic composition include female mate choice, changes in habitat associated with secondary succession, and, most strongly, a hierarchy of male territorial advantage—ecological mechanisms likely to be involved in the emergence and disappearance of many animal hybrid zones. Our results suggest that genetic assimilation is not a significant threat to either species and that rather transient hybrid zones such as this may serve to increase genetic diversity and are candidates for causing genetic discordance in phylogeographic analyses.

杂交（Hybridization）是一种重要的进化动力，可通过产生新物种并以多种途径影响亲本物种的演化，其中包括基因渐渗（introgression）与杂种优势（hybrid vigor）所带来的效应。然而，解析杂交带（hybrid zone）演化背后的生态过程颇具难度，因为这需要同时监测基因型频率（genotypic frequency）随时间的变化与对应的生态数据，而这类协同采集的数据集极为罕见。本研究描述了东部栅栏蜥蜴（Eastern Fence Lizard，*Sceloporus undulatus*）与佛罗里达灌丛蜥蜴（Florida Scrub Lizard，*Sceloporus woodi*）之间一处杂交带的遗传与生态特征，该杂交带的演化已持续至少23个世代。该杂交带于35年前通过形态特征（morphological character）被首次发现，最初亲本物种与杂交个体的占比近乎均等。如今，我们借助遗传标记（genetic marker）——涵盖物种特异性线粒体DNA（mitochondrial DNA）位点以及共计117个个体的6个核DNA（nuclear DNA）微卫星位点——不仅证实了杂交事件的发生，还发现后续回交（backcrossing）已产生高度基因渐渗的杂交个体：诸多杂交个体的核DNA背景源自一个物种，却携带另一物种的线粒体DNA。可解释这类遗传组成变化的生态因素包括雌性配偶选择（female mate choice）、与次生演替（secondary succession）相关的生境改变，其中影响最为显著的是雄性领地优势（male territorial advantage）层级——这类生态机制极可能参与了诸多动物杂交带的形成与消散过程。本研究结果表明，遗传同化（genetic assimilation）对这两个物种均未构成显著威胁；而此类临时性杂交带（transient hybrid zone）或可提升种群遗传多样性，同时也可能成为系统地理学分析（phylogeographic analysis）中出现遗传不一致性的潜在诱因。