Hooking the scientific community on thorny-headed worms: interesting and exciting facts, knowledge gaps and perspectives for research directions on Acanthocephala

Abstract

Although interest in Acanthocephala seems to have reached only a small community of researchers worldwide, we show in this opinion article that this group of parasites is composed of excellent model organisms for studying key questions in parasite molecular biology and cytogenetics, evolutionary ecology, and ecotoxicology. Their shared ancestry with free-living rotifers makes them an ideal group to explore the origins of the parasitic lifestyle and evolutionary drivers of host shifts and environmental transitions. They also provide useful features in the quest to decipher the proximate mechanisms of parasite-induced phenotypic alterations and better understand the evolution of behavioral manipulation. From an applied perspective, acanthocephalans’ ability to accumulate contaminants offers useful opportunities to monitor the impacts – and evaluate the possible mitigation – of anthropogenic pollutants on aquatic fauna and develop the environmental parasitology framework. However, exploring these exciting research avenues will require connecting fragmentary knowledge by enlarging the taxonomic coverage of molecular and phenotypic data. In this opinion paper, we highlight the needs and opportunities of research on Acanthocephala in three main directions: (i) integrative taxonomy (including non-molecular tools) and phylogeny-based comparative analysis; (ii) ecology and evolution of life cycles, transmission strategies and host ranges; and (iii) environmental issues related to global changes, including ecotoxicology. In each section, the most promising ideas and developments are presented based on selected case studies, with the goal that the present and future generations of parasitologists further explore and increase knowledge of Acanthocephala.

Diversity of Acanthocephala parasites in Neotropical amphibians

“…Thus, non-specific reports were very common. This aspect, coupled with the scarcity of specialists in the field (Perrot-Minnot et al 2023) and the inherent complexity of parasite identification (Selbach et al 2019;Zhao et al 2023), contributes to a taxonomic gap for acanthocephalans.…”

“…Acanthocephala is a monophyletic group exclusively comprising parasitic organisms. Phylogenetically, this group shares a relationship with rotifers, characterized by the presence of a syncytial epidermis (Storch and Welsch 1969;García-Varela and Nadler 2006;Perrot-Minnot et al 2023). The name Acanthocephala (acantho = spines, cephala = head) derives from the group's main morphological feature: a spiny proboscis at the anterior end of their body, through which they attach to host tissues.…”

Parasites and Pollutants: Effects of Multiple Stressors on Aquatic Organisms

“…The exclusively parasitic helminth group Acanthocephala is also called “thorny‐headed worms.” These parasites have life cycles that involve an invertebrate intermediate host (e.g., amphipods) and a vertebrate final host (e.g., fish; Kennedy, 2006; Perrot‐Minnot et al, 2023; see Figure 3 for details). The cystacanth larvae (Figure 3B) often manipulate the behaviour of their invertebrate intermediate host by interfering with host physiology to enhance the trophic transmission to the final host (Helluy, 2013) and thereby execute a variety of physiological effects (e.g., Bailly et al, 2018; Bakker et al, 2017; Bollache et al, 2000; Cornet, 2011), which might also be important for ecotoxicological studies (Grabner & Sures, 2019).…”

Pattern of anuran infection by acanthocephalans from the Cerrado, Northeastern Brazil with a summary for South America

“…In the context of the life cycle, Perrot-Minnot et al . (2023) point out the need to expand and disseminate knowledge on the range of hosts used by each acanthocephalan species. In the case of acanthocephalans, the degree of specificity varies between intermediate, paratenic, and definitive hosts and constitutes a crucial factor for the distribution and abundance of the parasite (Kennedy 2006).…”

“…Acanthocephalans comprise part of a model parasite–host system that requires studies on their life cycles, their transmission strategies, and their host exploitation, as well as factors that contribute to host specialisation (Perrot-Minnot et al . 2023). Due to the small number of described acanthocephalan species, they have received less attention compared to other groups of endoparasitic metazoans.…”