Department of Entomology, University of Kentucky, Lexington, KY 40546, USA.
BMC Evol Biol. 2012 Sep 10;12:175. doi: 10.1186/1471-2148-12-175.
Transitions in habitats and feeding behaviors were fundamental to the diversification of life on Earth. There is ongoing debate regarding the typical directionality of transitions between aquatic and terrestrial habitats and the mechanisms responsible for the preponderance of terrestrial to aquatic transitions. Snail-killing flies (Diptera: Sciomyzidae) represent an excellent model system to study such transitions because their larvae display a range of feeding behaviors, being predators, parasitoids or saprophages of a variety of mollusks in freshwater, shoreline and dry terrestrial habitats. The remarkable genus Tetanocera (Tetanocerini) occupies five larval feeding groups and all of the habitat types mentioned above. This study has four principal objectives: (i) construct a robust estimate of phylogeny for Tetanocera and Tetanocerini, (ii) estimate the evolutionary transitions in larval feeding behaviors and habitats, (iii) test the monophyly of feeding groups and (iv) identify mechanisms underlying sciomyzid habitat and feeding behavior evolution.
Bayesian inference and maximum likelihood analyses of molecular data provided strong support that the Sciomyzini, Tetanocerini and Tetanocera are monophyletic. However, the monophyly of many behavioral groupings was rejected via phylogenetic constraint analyses. We determined that (i) the ancestral sciomyzid lineage was terrestrial, (ii) there was a single terrestrial to aquatic habitat transition early in the evolution of the Tetanocerini and (iii) there were at least 10 independent aquatic to terrestrial habitat transitions and at least 15 feeding behavior transitions during tetanocerine phylogenesis. The ancestor of Tetanocera was aquatic with five lineages making independent transitions to terrestrial habitats and seven making independent transitions in feeding behaviors.
The preponderance of aquatic to terrestrial transitions in sciomyzids goes against the trend generally observed across eukaryotes. Damp shoreline habitats are likely transitional where larvae can change habitat but still have similar prey available. Transitioning from aquatic to terrestrial habitats is likely easier than the reverse for sciomyzids because morphological characters associated with air-breathing while under the water's surface are lost rather than gained, and sciomyzids originated and diversified during a general drying period in Earth's history. Our results imply that any animal lineage having aquatic and terrestrial members, respiring the same way in both habitats and having the same type of food available in both habitats could show a similar pattern of multiple independent habitat transitions coincident with changes in behavioral and morphological traits.
生境和摄食行为的转变是地球上生命多样化的基础。关于水生和陆生生境之间转变的典型方向以及导致陆生向水生转变占优势的机制，目前仍存在争议。食蜗牛蝇（双翅目：Sciomyzidae）是研究此类转变的绝佳模式系统，因为其幼虫表现出一系列摄食行为，是淡水、海岸线和干燥陆地生境中各种软体动物的捕食者、寄生者或腐生者。非凡的 Tetano cer a 属（Tetanocerini）占据了五个幼虫摄食群，以及上述所有生境类型。本研究有四个主要目标：（i）为 Tetano cer a 和 Tetanocerini 构建一个稳健的系统发育估计，（ii）估计幼虫摄食行为和生境的进化转变，（iii）测试摄食群的单系性，以及（iv）确定 Sciomyzid 生境和摄食行为进化的机制。
基于分子数据的贝叶斯推断和最大似然分析强烈支持 Sciomyzini、Tetanocerini 和 Tetano cer a 是单系的。然而，通过系统发育约束分析，许多行为分组的单系性被拒绝。我们确定，（i）祖先的食蜗牛蝇谱系是陆生的，（ii）在 Tetanocerini 的进化早期发生了一次单一的陆生向水生生境的转变，（iii）在 Tetanocerine 系统发育过程中至少发生了 10 次独立的水生向陆生生境的转变和至少 15 次摄食行为的转变。Tetano cer a 的祖先为水生，有五个谱系独立向陆生生境过渡，七个谱系独立向摄食行为过渡。
食蜗牛蝇中水生向陆生转变的优势与整个真核生物中普遍观察到的趋势背道而驰。潮湿的海岸线生境可能是过渡性的，幼虫可以改变生境，但仍有类似的猎物。对于食蜗牛蝇来说，从水生向陆生生境的转变比相反的转变更容易，因为与在水面下呼吸有关的形态特征会丢失而不是获得，并且食蜗牛蝇起源和多样化发生在地球历史上一个普遍干燥的时期。我们的结果表明，任何具有水生和陆生成员的动物谱系，如果在两个生境中以相同的方式呼吸，并且在两个生境中都有相同类型的食物，都可能表现出类似的模式，即多个独立的生境转变与行为和形态特征的变化同时发生。
