Widespread and persistent invasions of terrestrial habitats coincident with larval feeding behavior transitions during snail-killing fly evolution (Diptera: Sciomyzidae)

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.

The State of Phylogenetic Analysis: Narrow Visions and Simple Answers—Examples from the Diptera (flies)

“…The other is to ensure that the broader community is aware that not all studying dipteran phylogenetics consider the Wiegmann et al (2011) results as anything remotely close to a "Periodic Table" of Diptera relationships. These results certainly are not authoritative and should not to be used as a template for further study, as has been done by many, with almost 400 citations as of this writing (e.g., Chapman et al, 2012;Dijkstra et al, 2014;Espíndola et al, 2012;Friedemann et al, 2014;Tkoč et al, 2016;Mitterboeck et al, 2016;Nagler & Haug, 2015;Pape et al, 2011;Rotheray & Lyszkowski, 2015;Schneeberg et al, 2013;Vicoso & Bachtrog, 2015).…”

“…Group after group is being sequenced and the resultant phylogenies abound (e.g., Buenaventura et al, 2016;Caravas & Friedrich, 2013;Chapman et al, 2012;Ding et al, 2015;Haseyama et al, 2015;Semelbauer, 2016;Ševčík, 2016;Wang et al, 2016;Winkler et al, 2015;Winterton et al, 2016;Young et al, 2016a;. Molecular analyses are promising to give final answers (Trautwein et al, 2017;Yeates et al, 2016) and morphological analyses are often as straightforward as scoring variable character states in a matrix, choosing a few taxa as outgroups and determining the most parsimonious tree with a program (and options) of choice (usually PAUP or Mesquite + TNT).…”

Dictya behrmani, a New Species of Snail-Killing Fly (Diptera: Sciomyzidae) from Indiana

“…Larvae of most species attack aquatic, shoreline, or terrestrial species of snails and slugs. Exceptions include larvae of Renocera Hendel species, most of which (Chapman et al 2012) attack fingernail clams, and early instars of Anticheta Haliday species, which feed within egg masses of pulmonate snails.…”

Rates and patterns of molecular evolution in freshwater versus terrestrial insects

“…Taxa labels: Neur., Neuroptera; Trichopt., Trichoptera; Mc, Mecoptera. Source studies used for phylogenetic topologies: Insecta backbone and Mecoptera: Misof et al 2014;Coleoptera: Bernhard et al 2006;Hunt et al 2007;Song et al 2014;Diptera: Brammer and von Dohlen 2007;Wiegmann et al 2011;Curler and Moulton 2012;Chapman et al 2012;Trichoptera: Hayashi et al 2008;Lepidoptera: Regier et al 2012;Rubinoff and Schmitz 2010;Hemiptera: Li et al 2012;Neuroptera: Aspöck et al 2012. Complete information on the source studies used for topologies and habitat information, and sources of molecular data, is provided in the supplementary data 2 .…”

“…Adult-life-stage habitat shifts (with the larvae inhabiting various environments, but mainly aquatic) have occurred within Coleoptera at least 10 times (Hunt et al 2007), including some reversions; at least five adult shifts have likely occurred in the Hemiptera as well (Carver et al 1991). Dipteran lineages have experienced many (20+) terrestrial-to-aquatic larval-stage transitions (plus many reversions) (Chapman et al 2012;Wiegmann et al 2011), as have Hymenoptera (wasps, bees, and ants) (Bennett 2008) and Lepidoptera (moths and butterflies) (Rubinoff and Schmitz 2010;Foottit and Adler 2009).…”