Figure 1. Hormaphis cornu aphids drive patterned over-proliferation of plant cells to produce galls on leaves Hamamelis virginiana.

(A-C) Photographs of the abaxial surfaces of H. virginiana leaves being attacked by first-instar fundatrices of H. cornu. Nymphs gather on the unopened leaf buds (A) and soon after bud break the fundatrices gather near leaf veins (B) and inject material that begins to transform the leaf into a gall (C). Magnified region in blue rectangle of panel (A) shows three fundatrices waiting on unopened bud (A’).

(D-F) Photographs of the adaxial leaves of H. virginiana, showing galls at early (D), middle (E), and late (F) growth stages.

(G-I) Confocal micrographs of sections through a H. cornu gall (G, H) and un-galled H. virginiana leaf (I) stained with Congo red and calcofluor white. Extensive hypertropy is observed in the mesophyll (yellow arrows) at a considerable distance from the location of the aphid’s stylets (blue arrows) (G). The tips of aphid stylets (pink arrow) can be observed within cells of H. virginiana and plant tissue shows evidence of hyperproliferation and periclinal divisions (grey arrows) close to the tips of stylets and the termini of stylet sheaths (H). Periclinal divisions are observed in both spongy and palisade mesophyll cells during gall development, but never in ungalled leaf tissue (I). Plant tissue is presented in the aphid’s frame of reference, with abaxial leaf surface up.

(J) Diagram of life cycle of H. cornu. H. cornu migrates annually between H. virginiana (blue line) and Betula nigra (pink line) and the gall is produced only in the spring on H. virginiana (brown line). Each nymph of the first generation (G1, the fundatrix) hatches from an over-wintering egg and initiates development of a single gall. Her offspring (G2) feed and grow within the gall and develop with wings, which allows them to fly to B. nigra in late spring. For three subsequent generations (G3-G5) the aphids develop as small, coccidiform morphs on B. nigra. In the fall, aphids develop with wings (G6), fly to H. virginiana plants, and deposit male and female sexuals (G7), the only generation possessing meiotic cells. The sexuals feed and complete development on the senescing leaves of H. virginiana. As adults they mate and the females deposit eggs that overwinter and give rise to fundatrices the following spring.

See also Video S1.