Collaborative research: Is hybridization among threatened Caribbean coral species the key to their survival or the harbinger of their extinction?

造礁的acroporid珊瑚构成了整个加勒比地区浅层热带珊瑚群落的基础。然而，自20世纪80年代以来，曾经占主导地位的鹿角珊瑚（Acropora cervicornis）和麋鹿珊瑚（A. palmata）已经减少了90%以上，主要原因是疾病。它们的持续减少危及珊瑚礁提供众多社会和生态效益的能力，包括海产品收获和旅游业的经济收入，以及保护海岸线免受风暴和飓风造成的极端海浪事件的影响。尽管自2006年以来，它们受到美国濒危物种法案的保护，但对造礁珊瑚的生存威胁仍然普遍存在，包括疾病和海洋温度升高，可能导致进一步的大规模死亡。然而，这些密切相关的物种之间的杂交正在增加，可能为适应不断变化的环境提供了一条途径。虽然杂交品种在过去很少见，但它们现在在极端温度和光照的浅生境中茁壮成长，并正在向亲本物种的栖息地扩张。另外的证据表明，这种杂交品种至少比亲本品种中的一种抗病能力更强。因此，杂交可能有可能通过与两个亲本物种交配的杂交基因转移来拯救濒临灭绝的亲本物种，但广泛的基因流动可能会改变亲本物种的进化轨迹，导致其中一个或两个物种灭绝。该合作项目旨在收集遗传和生态数据，以了解杂交丰度增加的机制。从这项研究中获得的知识将有助于在当前和新出现的威胁下对珊瑚种群进行更有战略意义的管理。该项目包括对高中生、本科生和研究生的综合研究和教育机会，以及博士后研究人员。美属维尔京群岛的学生将参加珊瑚产卵研究，资源管理人员将接受关于acroporid生殖的培训，以便将其应用于珊瑚恢复技术。目前的模型预测，由于海面温度上升和海洋酸化，珊瑚礁将在未来200年内消亡。因此，必须确定生境、分类群和进化机制，使一些珊瑚物种能够保持其作为基础动物群的作用。杂交可以为适应不断变化的环境提供一条途径。珊瑚以一定的频率杂交，结果可能从通过基因渗入将几个等位基因引入现有的亲本物种，到诞生一个新的，也许更适应的遗传谱系。唯一被广泛接受的珊瑚杂交系统是由曾经占统治地位但现在受到威胁的加勒比物种——鹿角珊瑚（Acropora cervicornis）和棕榈珊瑚（A. palmata）组成。在过去，由麋鹿珊瑚和鹿角珊瑚自然杂交产生的杂交群落是罕见的，杂交繁殖的证据仅限于与鹿角珊瑚的罕见交配。最近的实地观察表明，这种杂交品种正在增加，其在整个加勒比地区的生态作用正在发生变化。这些杂交品种似乎较少受到近几十年来导致其亲本物种大量死亡的疾病的影响。杂交物种也在温度高、光照强的浅生境中茁壮成长，这表明它们可能不太容易受到未来气候变暖的影响。与此同时，它们正在向更深处的亲本物种栖息地扩张。初步的遗传数据表明，杂交物种现在正在相互交配，这表明有可能形成一个新物种。此外，杂交珊瑚似乎能够与鹿角珊瑚和麋鹿珊瑚交配，这可能导致基因通过杂交物种在亲本物种之间流动。研究建议解决杂交的增加和可能随后的渗入将如何影响加勒比acroporids当前的生态作用和未来的进化轨迹。具体来说，这个合作项目旨在回答以下问题：1)跨物种范围和基因组的基因渗入的历史速度、方向和程度是什么？基于三个重复杂交区全基因组SNP基因分型的连锁块分析将回答这个问题。2)下一代混合地层的目前程度和未来潜力如何？形态计量学和遗传学分析结合体外受精分析将被使用。3)是什么机制让杂交体在炎热的浅水中茁壮成长？一系列的原位和非原位操作实验将确定生物或非生物因素是否有利于在浅水中杂交生存。4)杂交品种是否比亲本品种更具抗病性？将进行互惠移植实验中的疾病传播分析和确定疾病程度的组织学分析。将采取多学科方法，结合传统和尖端技术，对加勒比珊瑚的进化生态进行详细分析。

Reef-building acroporid corals form the foundation of shallow tropical coral communities throughout the Caribbean. Yet, the once dominant staghorn coral (Acropora cervicornis) and the elkhorn coral (A. palmata) have decreased by more than 90% since the 1980s, primarily from disease. Their continuing decline jeopardizes the ability of coral reefs to provide numerous societal and ecological benefits, including economic revenue from seafood harvesting and tourism and shoreline protection from extreme wave events caused by storms and hurricanes. Despite their protection under the U.S. Endangered Species Act since 2006, threats to the survival of reef-building acroporid corals remain pervasive and include disease and warming ocean temperatures that may lead to further large-scale mortality. However, hybridization among these closely related species is increasing and may provide an avenue for adaptation to a changing environment. While hybrids were rare in the past, they are now thriving in shallow habitats with extreme temperatures and irradiance and are expanding into the parental species habitats. Additional evidence suggests that the hybrid is more disease resistant than at least one of the parental species. Hybridization may therefore have the potential to rescue the threatened parental species from extinction through the transfer of adapted genes via hybrids mating with both parental species, but extensive gene flow may alter the evolutionary trajectory of the parental species and drive one or both to extinction. This collaborative project is to collect genetic and ecological data in order to understand the mechanisms underlying increasing hybrid abundance. The knowledge gained from this research will help facilitate more strategic management of coral populations under current and emerging threats to their survival. This project includes integrated research and educational opportunities for high school, undergraduate and graduate students, and a postdoctoral researcher. Students in the United States Virgin Islands will take part in coral spawning research and resource managers will receive training on acroporid reproduction to apply to coral restoration techniques. Current models predict the demise of reefs in the next 200 years due to increasing sea surface temperatures and ocean acidification. It is thus essential to identify habitats, taxa and evolutionary mechanisms that will allow some coral species to maintain their role as foundation fauna. Hybridization can provide an avenue for adaptation to changing conditions. Corals hybridize with some frequency and results may range from the introduction of a few alleles into existing parent species via introgression, to the birth of a new, perhaps better adapted genetic lineage. The only widely accepted coral hybrid system consists of the once dominant but now threatened Caribbean species, Acropora cervicornis and A. palmata. In the past, hybrid colonies originating from natural crosses between elkhorn and staghorn corals were rare, and evidence of hybrid reproduction was limited to infrequent matings with the staghorn coral. Recent field observations suggest that the hybrid is increasing and its ecological role is changing throughout the Caribbean. These hybrids appear to be less affected by the disease that led to the mass mortality of their parental species in recent decades. Hybrids are also found thriving in shallow habitats with high temperatures and irradiance suggesting they may be less susceptible to future warming scenarios. At the same time, they are expanding into the deeper parental species habitats. Preliminary genetic data indicate that hybrids are now mating with each other, demonstrating the potential for the formation of a new species. Further, hybrids appear to be capable of mating with both staghorn and elkhorn coral, perhaps leading to gene flow between the parent species via the hybrid. Research is proposed to address how the increase in hybridization and perhaps subsequent introgression will affect the current ecological role and the future evolutionary trajectory of Caribbean acroporids. Specifically, this collaborative project aims to answer the following questions: 1) What is the historic rate, direction, and degree of introgression across species ranges and genomes? Linkage block analysis based on genome-wide SNP genotyping across three replicate hybrid zones will answer this question. 2) What is the current extent and future potential of later generation hybrid formation? Morphometric and genetic analyses combined with in vitro fertilization assays will be used. 3) What mechanisms allow hybrids to thrive in hot, shallow waters? A series of manipulative in situ and ex situ experiments will determine whether biotic or abiotic factors favor hybrid survival in shallow waters. 4) Are hybrids more disease resistant than the parentals species? Disease transmission assays in reciprocal transplant experiments and histological analysis to determine the extent of disease will be conducted. A multidisciplinary approach will be taken that combines traditional and cutting edge technology to provide a detailed analysis of the evolutionary ecology of Caribbean corals.