Among the families of Lepidoptera, Mitter et al. (2017) considered that Micropterigidae is probably the basal lineage but said that “the question is not fully settled.” If correct, however, then they concluded that the gymnosperm-seed-feeding family Agathiphagidae is the next successive family in the order and the sister family of all other Lepidoptera, the clade Angiospermavora. The phylogenomic study of Kawahara et al. (2019) supported these relationships.

Larvae of micropterigids feed on foliose liverworts, mosses, or detritus and live in or on the ground (Mitter et al. 2017) without constructed cases or shelters (i.e., are “free living”). Davis and Landry (2012) provided further details for two of the three species of the North American micropterigid genus Epimartyria: E. auricrinella Walsingham, 1898, and E. pardella (Walsingham 1880). Epimartyria auricrinella larvae feed on liverworts (Bazzania trilobata) in shaded, wet locations (swampy woods, boggy ditches, creek margins), “which probably differed little from those of ancestral ‘Amphiesmenoptera’ ” (Kristensen 1997), and that can be flooded periodically or seasonally. They are peripneustic with spiracles on abdominal segments I–VIII and a plastron supporting a thin layer of air on each side around the spiracles and over the posterior pronotum, permitting survival when submerged for at least short periods. Eggs of E. pardella are laid on the ventral surfaces of liverwort (Conocephalum conicum) and larvae also spend days on the undersides of liverwort thalli; “pupation occurs within a thin-walled, tightly woven brown cocoon close to the ground and attached to vegetation with strands of coarse silk” (Davis and Landry 2012); no other pupal shelter was mentioned. For basal lineages of Lepidoptera, silk production is confined to construction of cocoons by last-instar larvae (Kristensen 1997).

In multigene and phylogenomic studies, Thomas et al. (2020), Frandsen et al. (2024), and Ge et al. (2024a) all concluded that Trichoptera and suborders Annulipalpia and Integripalpia are each monophyletic. Furthermore, they concluded that the relationships within Annulipalpia were (Hydropsychoidea (Philopotamoidea + Psychomyioidea). Within Integripalpia, those three studies also concluded that the basal lineage is a clade of Hydroptiloidea sister families Ptilocolepidae and Hydroptilidae (or Hydroptilidae only, Ptilocolepidae having not been studied by Ge et al. 2024a). Frandsen et al. (2024) and Ge et al. (2024a) also inferred that the remaining families of Integripalpia are a clade with relationships (Phryganides (Glossosomatidae + Rhyacophiloidea)), for which subterorder Phryganides Latreille, 1805, consists of all families with tube-case-making larvae.

In modern Annulipalpia, campodeiform larvae usually construct silken retreats in all instars to provide physical protection from predators, usually attached to stable substrate surfaces in lotic waterways. These retreats may be augmented with specialized filter nets to one side of the upstream end (Hydropsychoidea and Stenopsychidae) or much of the inner surface of the retreat itself may filter food particles (Philopotamidae and some Psychomyioidea). Some Psychomyioidea larvae use their retreats as snares resembling spider webs for capturing drifting prey, as lairs from which to pounce on unsuspecting prey or to graze on periphyton, as reinforcement for subterranean tunnels with filter nets (Wiggins 2004), or as substrate for culturing algae (Ings et al. 2010, 2017).

In modern Integripalpia, Hydroptiloidea (Hydroptilidae + Ptilocolepidae) larvae undergo hypermetamorphosis, with the first four instars having a typical campodeiform shape (Nielsen 1948) and then, in the fifth and final instar, becoming hypergastric, developing a much-enlarged abdomen. Notably, the early-instar campodeiform larvae are “free-living,” with only the last instar constructing a sagitally compressed or transversely depressed case of silk or of silk and plant or mineral substrate sealed laterally on two longitudinal seams; this case is usually portable but sometimes fixed to substrate (Wiggins 2004). In particular, much like at least some lepidopteran micropterigid larvae, Ptilocolepidae larvae shred living mosses and liverworts in hygropetric or madicolous, damp streamside habitats, typically above the water line. Furthermore, the final instar, with its much-enlarged abdomen, constructs a portable, transversely depressed case of pieces of liverwort (Thienemann 1904; Ito and Higler 1993; González et al. 2000; Wiggins 2004; Ito et al. 2014). The final instar of a hydroptiloid larva pupates in a silken cocoon that is either semipermeable (Hydroptilidae) or permeable (Ptilocolepidae) (Wiggins 2004).

In all larval instars, Glossosomatidae larvae construct so-called “tortoise” cases of mineral pieces from which they graze periphyton off the upper surfaces of rocks in rapidly flowing water. Each glossosomatid case consists of a dome-like dorsal covering attached laterally to a flat, transverse, ventral strap or “plastron” that leaves identical, interchangeable openings for the head and legs at one end and the tip of the abdomen at the other; prior to pupation, the fifth (last) larval instar removes the ventral strap, seals the remaining dome to the rock, and spins a semipermeable cocoon beneath it (Wiggins 2004). Campodeiform Rhyacophiloidea (Hydrobiosidae + Rhyacophilidae) larvae build no cases until just prior to pupation but roam freely over the substrate; they feed generally as predators, but sometimes scrape periphyton, collect fine particulate organic matter, or shred living plant tissue (Cummins et al. 2019). The dome-like shelter built by the mature larva resembles that of Glossosomatidae, under which the rhyacophiloid larva also spins a semipermeable cocoon before pupating (Wiggins 2004).

Tube-case making Phryganides larvae typically construct their cases in all instars. The earliest lineages of infraorder Plenitentoria Weaver, 1984, do so with angiosperm pieces and those of infraorder Brevitentoria Weaver, 1984, make cases with mineral materials. When preparing for pupation, they usually attach their larval cases to stable substrate and close the ends with tough silken mesh sieves to deter predators while allowing flow of oxygenated water (Wiggins 2004).

With apparent radiation of so much structural and functional diversity in freshwater ecosystems, we were curious to learn how the ancestral caddisfly larva invaded its aqueous habitat and what evolutionary adaptations allowed it to succeed in that environment.

Based on their phylogenomic analyses, both Frandsen et al. (2024) and Ge et al. (2024a) agreed that the ancestral larva of Integripalpia in all instars and probably of Trichoptera in at least early instars was “free-living,” i.e., without a portable case or fixed retreat. Now, by comparing the functional traits of the larva of the hypothesized basal lepidopteran lineage (Micropterigidae) and those of modern caddisfly lineages as summarized above, we can infer some additional functional traits of larvae of their Amphiesmenopteran ancestor and the Trichoptera ancestor and of the evolutionary route taken by the Trichoptera ancestor to invade freshwater habitats.

Our analysis concludes that larvae of the free-living caddisfly ancestor probably fed on bryophytes, as those of Micropterigidae and Ptilocolepidae do today. Bryophytes (liverworts, hornworts, mosses) require moist environments for reproduction and are often found living in or immediately beside flowing water and subject to immersion, attached by rhizomes to rocks and other stable substrate on stream edges (Glime 2023). Clinging to or sprawling on semiaquatic bryophytes was probably the common lifestyle of the caddisfly larval ancestor and may have been that of the amphiesmenopteran ancestor as well. The analysis indicated that lotic-erosional or terrestrial habitats are also possibilities. Whatever its habitat may have been, this ancestral caddisfly larva lost its spiracles and either lost or never had a plastron, respiring instead directly through its integument from the cold, oxygen-rich water, apparently making the terrestrial habitat option unlikely. This evolutionary development may also have been possible because of their small size and consequent high surface-to-volume ratio, allowing effective respiration in a freshwater medium. Thus, this ancestral caddisfly larva evolved from a semiterrestrial environment (as in Micropterigidae and Ptilocolepidae) into a permanently submerged lifestyle (as in most Hydroptiloidea and other Trichoptera), radiating to access the many food and habitat resources available under water in the Permian Period.

Precocious production of silk by the active larva, well before time for pupation, apparently evolved for various purposes in the ancestral Trichoptera larva, whether for retreat building (as in modern Annulipalpia) or larval case construction (as in most modern Integripalpia). The primitive caddisfly larva also constructed, apparently for the first time in Amphiesmenoptera, a dome-like pupation shelter of silk and substrate materials, an evolutionary development or synapomorphy of Trichoptera that is observed in basal lineages of both Annulipalpia and Integripalpia. The larva then spun a closed permeable or semipermeable cocoon inside this shelter, fusing the cocoon to its inner walls (Hydroptilidae) or leaving it mostly free (other basal lineages of modern Integripalpia), or the larva spun an open or closed cocoon as in modern Annulipalpia. In Integripalpia, larvae of the tube-case-making Phryganides pupated in their tube cases after lining them with silk and constructing tough silken mesh at either end, then making undulating ventilation movements to propel the unidirectional flow of water through the tube (Wiggins 2004).

Considering the recently published phylogenetic hypotheses (Thomas et al. 2020; Frandsen et al. 2024; Ge et al. 2024a), semipermeable cocoons may have evolved independently in Hydroptilidae and the Glossosomatidae + Rhyacophiloidea lineage; alternatively, semipermeable cocoons may have first appeared in the Integripalian ancestor and been abandoned in the Ptilocolepidae lineage and Phryganides. A further development in the Integripalpia lineage was the precocious construction of the pupal shelter in early instars (immediately on molting into the hypogastric last instar of Hydroptiloidea and in all instars of Glossosomatidae). Wiggins (2004) suggested that the hydroptiloid purse case and glossosomatid tortoise case are homologous because they are both based on two sheets of case materials fastened together at lateral seams; if these case-construction behaviors are homologous, the precocious construction of a pupal shelter apparently was abandoned in Rhyacophiloidea to facilitate rapid movement for capturing prey, delaying shelter construction until immediately before pupation; if they are not homologous, as Frandsen et al. (2024) concluded, the larval ancestor of Glossosomatidae+Rhyacophiloidea apparently was free-living, with the Glossosomatidae ancestor evolving tortoise case construction behavior independently.

The portable tubular cases of Phryganides larvae do not appear to be homologous with the portable cases of Hydroptiloidea and/or Glossosomatidae (Wiggins 2004). Nevertheless, this tubular type of case may also, like those of hydroptiloids and glossosomatids, have evolved as a precocious pupation shelter, initially for larval protection. For pupation, the tubular case was retained and modified by the production of silken sieve plates at the vulnerable ends, or the larval case was abandoned and a new protective tube shelter was constructed as in Phryganopsyche (Phryganopsychidae), Yphria (Phryganeidae), and Ecclisomyia (Limnephilidae) (Wiggins 2004; Givens 2018). Besides its value as camouflage and physical protection, a selective advantage of the tube was for improved respiration by larval and pupal undulations inside the tube, continuously directing a fresh supply of oxygenated water over the body. This adaptation allowed various lineages of Phryganides to invade quiet-water habitats with lower concentrations of dissolved oxygen (Mackay and Wiggins 1979). Most case-making larvae of basal Integripalpia included minerals of various sizes or filamentous algae into their larval/pupal cases. The incorporation of angiosperm leaf pieces in some later lineages, especially in earlier lineages of infraorder Plenitentoria, became possible after the evolution of that major plant clade (Morse et al. 2019).

Like the larvae of Rhyacophiloidea and early instar larvae of Hydroptiloidea, the larvae of most Annulipalpia have a campodeiform shape. They also evolved strong anal prolegs and tarsal claws for maneuvering efficiently on the substrate. Hydropsychidae are presently thought to be the basal lineage of Annulipalpia (Frandsen et al. 2024; Ge et al. 2024a) and species of their subfamily Arctopsychinae are considered the descendants of the basal lineage of Hydropsychidae (Geraci et al. 2005). Modern species of Arctopsychinae characteristically live in some of the fastest flowing mountain-stream habitats. The functional changes that allowed a free-living, wet-habitat ancestral caddisfly larva to invade lotic-erosional ecotones characteristically occupied by modern arctopsychines are unclear and must have been dramatic, a scenario inviting future investigation.