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.

Comparing ant morphology measurements from microscope and online AntWeb.org 2D z‐stacked images

“…It is also a favored source of data to pursue questions in morphological evolution (Dehon et al, 2014;Lawing & Polly, 2010;Wagner et al, 2018), and constitutes a sound methodology for detecting allometries in developmental biology (Chiu et al, 2015;Demuth et al, 2012;Laciny, 2021). Even in the era of rapidly advancing DNA sequencing technologies (Luo et al, 2018;Puillandre et al, 2012;Rannala & Yang, 2020), morphometry retains its prestige, as this approach is considered one of the most promising ways to find links between molecular conclusions and name-bearing types, that is, zoological nomenclature (Alitto et al, 2019;Renner et al, 2018).…”

“…Indeed, morphometrics, one of the most widely used quantitative approaches to studying morphology, has long been a popular approach in taxonomy and systematics (e.g., Baur et al, 2014 ; Christodoulou et al, 2020 ; Johnson et al, 2018 ; Longino & Branstetter, 2020 ; Michaloudi et al, 2018 ; Wagner et al, 2017 ). It is also a favored source of data to pursue questions in morphological evolution (Dehon et al, 2014 ; Lawing & Polly, 2010 ; Wagner et al, 2018 ), and constitutes a sound methodology for detecting allometries in developmental biology (Chiu et al, 2015 ; Demuth et al, 2012 ; Laciny, 2021 ). Even in the era of rapidly advancing DNA sequencing technologies (Luo et al, 2018 ; Puillandre et al, 2012 ; Rannala & Yang, 2020 ), morphometry retains its prestige, as this approach is considered one of the most promising ways to find links between molecular conclusions and name‐bearing types, that is, zoological nomenclature (Alitto et al, 2019 ; Renner et al, 2018 ).…”

Anatomy and evolution of the head of Dorylus helvolus (Formicidae: Dorylinae): Patterns of sex‐ and caste‐limited traits in the sausagefly and the driver ant

“…Previously, the only other aberrant muscle observed was functionless fibers of 0md1 in a Formica rufa Linnaeus, 1761 worker that attached to the dorsal and ventral surfaces of the cranium (Richter et al, 2020). Because muscular teratology in ants has not yet been a focal point of study, in contrast to external anatomy (e.g., Laciny, 2021; Sokolowski & Wisniewski, 1975), we suggest three alternative hypotheses to investigate at finer scale: (null) aberrant muscles occur purely by chance developmental misspecification (i.e., by pure “mistake”); (1) parasites or larval trauma; or (2) relaxed ecological selection on males may allow for accumulation of loss of function mutations. High throughput scanning and reconstruction of ants may be the best way to quantify these occurrences.…”

From Parasitized to Healthy-Looking Ants (Hymenoptera: Formicidae): Morphological Reconstruction Using Algorithmic Processing

“…These might also be alternative phenotypes of a known species developed in response to various environmental factors [ 7 , 8 ], including parasitism [ 9 ]. Some parasites of ants and many other insects are known to alter morphological traits of their hosts to various extents, from limited morphological shifts in a single trait to complete shape-shifts that alter many traits simultaneously [ 10 ]. Polyphenism (i.e., the ability to develop multiple discrete phenotypes from a single genotype) is the hallmark of every ant species.…”

“…In addition, we assessed the frequency distribution of both infected and uninfected individuals. The Temnothorax -Cestoda system is undoubtedly an excellent testing ground for our purpose because (i) this infection is well-known for myrmecologists [ 10 , 13 , 20 , 21 , 22 ], (ii) the infected ants are easy to identify in the field; the infection causes faded coloration in Temnothorax ants, turning individuals from a typical brown color to a yellowish one [ 23 ], and (iii) these parasites are expected to cause similar alternative morphologies across many host species, as is the case with nematode worms in Myrmica ants [ 12 , 18 ]. Finally, (iv) Temnothorax colonies are monogynous, so colony members are mostly full sisters.…”