Abstract
BackgroundTransitions 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.ResultsBayesian 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.ConclusionsThe 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.
Highlights
Transitions in habitats and feeding behaviors were fundamental to the diversification of life on Earth
All genera with multiple species are monophyletic except for (1) Limnia, which is rendered polyphyletic by Trypetoptera and Pherbina in the Bayesian inference (BI) MAP tree and by Trypetoptera in the best maximum likelihood (ML) tree, (2) Trypetoptera, rendered polyphyletic by Limnia ottawensis in both trees and (3) Renocera, rendered polyphyletic by Ethiolimnia and Dichetophora in both trees
We found the optimal ratio of aquatic-to-terrestrial vs. terrestrial-toaquatic transitions was between 11:1 and 13:1 which was significantly better than the null model with no bias in habitat transition rates and congruent with the Mesquite optimization
Summary
Transitions in habitats and feeding behaviors were fundamental to the diversification of life on Earth. Some of the most important evolutionary innovations in the history of life on Earth resulted from transitions between aquatic (freshwater) and terrestrial habitats. Whereas the ancestral insect originated in a terrestrial environment [10,11,12], insects are one of the most successful colonizers of freshwater habitats, as at least 12 of the 31 insect orders have representatives occupying these environments during at least one life history stage [13]. In order to transition between these habitats, a lineage typically must adapt to new physical conditions while concomitantly modifying its feeding behaviors
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