Among the shapeshifters: parasite-induced morphologies in ants (Hymenoptera, Formicidae) and their relevance within the EcoEvoDevo framework

Abstract

As social insects, ants represent extremely interaction-rich biological systems shaped by tightly integrated social structures and constant mutual exchange with a multitude of internal and external environmental factors. Due to this high level of ecological interconnection, ant colonies can harbour a diverse array of parasites and pathogens, many of which are known to interfere with the delicate processes of ontogeny and caste differentiation and induce phenotypic changes in their hosts. Despite their often striking nature, parasite-induced changes to host development and morphology have hitherto been largely overlooked in the context of ecological evolutionary developmental biology (EcoEvoDevo). Parasitogenic morphologies in ants can, however, serve as "natural experiments" that may shed light on mechanisms and pathways relevant to host development, plasticity or robustness under environmental perturbations, colony-level effects and caste evolution. By assessing case studies of parasites causing morphological changes in their ant hosts, from the eighteenth century to current research, this review article presents a first overview of relevant host and parasite taxa. Hypotheses about the underlying developmental and evolutionary mechanisms, and open questions for further research are discussed. This will contribute towards highlighting the importance of parasites of social insects for both biological theory and empirical research and facilitate future interdisciplinary work at the interface of myrmecology, parasitology, and the EcoEvoDevo framework.

Keywords: Cestoda; EvoDevo; Mattesia; Morphology; Myrmicinosporidium; Nematoda; Parasitology; Review; Social insects.

Fig. 1

Ants as hosts of Mermithidae: a Lasius niger mermithogyne with mermithid erupting from gaster, note shortened wings (from [51]); b Colobopsis sp. “nrSA”, mermithogenic intercaste, note wing stubs and black colour (from [52]); c microCT image of same specimen, mermithid visible in gaster (from [52]); d Camponotus pompeijus mermithergate, mermithid visible in gaster (from [50])

Fig. 2

Cephalotes atratus infected by Myrmeconema neotropicum: a infected C. atratus worker with berry-like gaster (left), healthy worker (right); b M. neotropicum mating pair (male top, female bottom) (photos: S.P. Yanoviak)

Fig. 3

Ant–parasitic Nematoda of the families Allantonematidae (a) and Seuratidae (b): a Formicitylenchus oregonensis from host Camponotus vicinus; b Rabbium paradoxus adults with host Camponotus castaneus (photos from [42], provided by G. Poinar)

Fig. 4

Temnothorax nylanderi infected by the dilepidid cestode Anomotaenia brevis; infected worker (top, note yellow colour) with healthy nestmate (bottom) (photo: S. Foitzik)

Fig. 5

Mattesia sp. infecting Solenopsis invicta: a infected alate gyne of S. invicta surrounded by workers, note yellow head and thorax signifying “yellow-head disease”; b Mattesia sp. spores visible though cuticle of infected ant; c characteristic pair of lemon-shaped spores (photos: R. Pereira)

Fig. 6

Pheidole nodus infected by Myrmicinosporidium durum: a minor worker, lateral view, note visible spores in gaster, petiole, mesosoma and coxae; b electron microscopic image of opened gaster, note lentil-shaped spores (photos: S. Hosoishi)

Fig. 7

Labial gland disease in Formica polyctena; healthy queen (top left; colour bleached by storage in ethanol), healthy worker (top right), and two “pseudogyne” or “secretergate” specimens with labial gland disease (bottom, note humped mesosoma) (photo from [161])

Fig. 8

Summary of evolutionary and developmental factors mentioned in the literature surrounding parasite-induced phenotypes in ants; preimaginal parasitic infection (left box) may cause developmental perturbations (middle box), which are mediated by properties of individual ontogeny (clear arrows) as well as colony-level factors (grey arrows). This results in phenotypic changes to the host (right box), which may in turn mutually interact with further individual and colony-level evolutionary and developmental processes (photos: S.P. Yanoviak, R. Pereira, A. Laciny, [52])