Between extreme simplification and ideal optimization: antennal sensilla morphology of miniaturized Megaphragma wasps (Hymenoptera: Trichogrammatidae)

One of the major trends in the evolution of parasitoid wasps is miniaturization, which has produced the smallest known insects. Megaphragma spp. (Hymenoptera: Trichogrammatidae) are smaller than some unicellular organisms, with an adult body length of the smallest only 170 µm. Their parasitoid lifestyle depends on retention of a high level of sensory reception comparable to that in parasitoid wasps that may have antennae hundreds of times larger. Antennal sensilla of males and females of Megaphragma amalphitanum and M. caribea and females of the parthenogenetic M. mymaripenne are described, including sensillum size, external morphology, and distribution. Eight different morphological types of sensilla were discovered, two of them appearing exclusively on female antennae. Two of the types, sensilla styloconica and aporous placoid sensilla, have not been described previously. Regression analyses were performed to detect and evaluate possible miniaturization trends by comparing available data for species of larger parasitoid wasps. The number of antennal sensilla was found to decrease with the body size; M. amalphitanum males have only 39 sensilla per antenna. The number of antennal sensilla types and sizes of the sensilla, however, show little to no correlation with the body size. Our findings on the effects of miniaturization on the antennal sensilla of Megaphragma provide material for discussion on the limits to the reduction of insect antenna

External morphology of <i>Megaphragma mymaripenne</i>, SEM.

<p>(A) Dorsal view; (B) Lateral view; (C) Ventral view.</p

Musculature of head in <i>Megaphragma mymaripenne</i>, 3D.

<p>(A–C) Lateral internal view; (D) Lateral external view; (E) Dorsal view; (F) Frontal view; ant–antenna, ata–anterior tentorial arms, lb–labium, md–mandible, mx–maxilla, oc–eye, ocl–ocellus, ph–pharynx. Musculature see text.</p

Internal morphology of <i>Megaphragma mymaripenne</i>, 3D (for interactive version see S1 Fig).

<p>(A) Lateral internal view; (B) Lateral external view; (C) Dorsal view; (D) Ventral view; acg–acid gland, ag–abdominal ganglion, cer–cerebrum, cx1.2 –meso- and metacoxae, exv–external valves of ovipositor, gg1.2.3 –pro-, meso-, and metathoracic ganglia, fr2 –mesophragma; mg–midgut, mt–Malpighian tubules, oc–eye, oes–oesophagus, ova–ovary, rc–rectum, soeg–suboesophageal ganglion, stl–stylet of ovipositor. Colors: blue–cuticle, green–digestive system, yellow–central nervous system, brown–musculature, purple–reproductive system. Musculature see text.</p

Ultrastructure of the brain in <i>Megaphragma</i>, TEM.

<p>(A, C, D) <i>M</i>. <i>mymaripenne</i>; (B, E, F) <i>M</i>. <i>amalphitanum;</i> mt ‒ mitochondrion, np–neuropil, nu ‒ nucleus.</p

Internal morphology of <i>Megaphragma amalphitanum</i>.

<p>(A) Scheme of sections, lateral view; (B–F) Longitudinal sections, DAPI and autofluorescence; ag–abdominal ganglion, cer–cerebrum, gg1,2,3 –pro-, meso-, and methatoracic ganglion, ova–ovary. Musculature see text.</p

Structure of head in <i>Megaphragma mymaripenne</i>, SEM.

<p>(A–C) Head; (A) Dorsal view; (B) Lateral view; (C) Frontal view; (D) Antennae; (E) Mouthparts, posterior view; (F) Mouthparts, ventral view; ant–antenna, ca–cardo, cuf–cuticular folds, ga–galea, lbp–labial palp, li–ligula, md–mandible, mxp–maxillary palp, oc–eye, ocl–ocellus, prm–prementum, sr–sensory ridge, sti–stipes.</p

Structure of meso- and of metasoma in <i>Megaphragma</i>, SEM.

<p>(A–F, H) <i>M</i>. <i>mymaripenne</i>; (G) <i>M</i>. <i>amalphitanum</i>; (A–C) Mesosoma; (D) Apex tarsi; (E–G) Metasoma; (H) Wing setae; (A, H) Dorsal view; (B, D) Ventral view; (C, D, F, G) Lateral view; aed–aedeagus, aest2 –mesepistern, aest3 –metepisternum, aro–arolium, ax–axillary sclerite, cl–claw, cx1.2.3 –pro-, meso-, and metacoxae, ep2 –mesepimeron, exv–external valves of ovipositor, inv–internal valves of ovipositor, ll–scapulae, nt1.3 –pro- and metanotum, par–parameres, pl1 –pleurite of prothorax, pre–prepectus, pro–propodeum, prp–propectus, sc–scutum, scl–scutellum, sp–spiracle, stl–stylet of ovipositor, ter–tergite, wi–wing.</p

Anatomy of adult <i>Megaphragma</i> (Hymenoptera: Trichogrammatidae), one of the smallest insects, and new insight into insect miniaturization

<div><p>The body size, especially in cases of extreme reduction, is an important characteristic that strongly determines the morphology, physiology, and biology of animals. Miniaturization is a widespread trend in animal evolution and one of the principal directions of evolution in insects. Miniaturization-related features of insect morphology have been subject to intensive studies during the last few years, but the structure of the smallest insects remains insufficiently known. It is especially important to study hymenopterans of the genus <i>Megaphragma</i>, which include the smallest flying insects and a species in which an almost anucleate nervous system was recently discovered. This article is the first detailed study of the external and internal morphology of adults of <i>Megaphragma mymaripenne</i> and <i>M</i>. <i>amalphitanum</i> using histological methods, 3D computer modeling and other techniques. It is shown that in spite of the extremely small size the organization of <i>Megaphragma</i> retains a considerkable level of structural complexity. On the other hand, miniaturization leads to re-organizations of several organ systems. Unique structural features related to miniaturization have been found in both species: lysis of cell bodies and nuclei of neurons at late stages of pupal development, absence of the heart, and considerable reductions in the set of muscles. Comparative analysis of structure in the smallest insects representing different taxa has revealed common features of the evolutionary process of miniaturization in insects.</p></div

Anatomy of adult <i>Megaphragma</i> (Hymenoptera: Trichogrammatidae), one of the smallest insects, and new insight into insect miniaturization - Fig 9

<p><b>Musculature of mesosoma in <i>Megaphragma mymaripenne</i>, 3D/</b> (A–C) Lateral internal view; (D) Lateral external view; (E) Dorsal view; (F) Ventral view; pl1 –pleurite of prothorax, pla3 –pleural apodeme of metathorax, fr1.2 –pro- and mesophragma, fu1.2 –pro- and mesofurca, cx1.2.3 –pro-, meso-, and metacoxae. Musculature see text.</p