Insights on the host associations and geographic distribution of Hymenolepis folkertsi (Cestoda: Hymenolepididae) among rodents across temperate latitudes of North America

Abstract

Synoptic data and an understanding of helminth parasite diversity among diverse rodent assemblages across temperate latitudes of North America remain remarkably incomplete. Renewed attention to comprehensive survey and inventory to establish the structure of biodiverse faunas is essential in providing indicators and proxies for identifying the outcomes of accelerating change linked to climate warming and anthropogenic forcing. Subsequent to the description of Hymenolepis folkertsi in the oldfield mouse, Peromyscus polionotus, additional specimens of hymenolepidids were collected or discovered in archived museum repositories from multiple species of deer mice (Peromyscus maniculatus, Peromyscus leucopus), the golden mouse (Ochrotomys nuttalli), chipmunks (Tamias striatus, Tamias amoenus), the 13-lined ground squirrel (Ictidomys tridecemlineatus), and tree squirrels (Sciurus carolinensis, Sciurus niger) from disjunct localities in the USA spanning southern Georgia, Virginia, Pennsylvania, Connecticut, the Upper Peninsula of Michigan, Wisconsin, and central Idaho. Specimens were largely consistent morphologically with the original description of H. folkertsi. Initial DNA sequence data, from a portion of the mitochondrial NADH dehydrogenase subunit 1, demonstrated intraspecific variation among three apparently geographically isolated populations attributed to H. folkertsi (uncorrected genetic distances of 2.7 % (Idaho and Michigan), 2.4 % (Virginia + Pennsylvania and Michigan), and 1.89 % (VA + PA and ID). Geography rather than host association explains the distribution and occurrence of H. folkertsi, and host colonization among deer mice, chipmunks, and other sciurids within regional sites is indicated. Genetic divergence revealed across localities for H. folkertsi suggests historically isolated populations, consistent with extended evolutionary and biogeographic trajectories among hymenolepidids and species of Peromyscus and Tamias in North America. Field inventory, that revealed these parasite populations, substantially alters our understanding of the distribution of diversity and provides insights about the nature of the complex relationships that serve to determine cestode faunas in rodents.

Hymenolepis ackerti n. sp. (Eucestoda: Hymenolepididae) infecting cricetid rodents from the central Great Plains of North America

“…Perhaps the only three species featuring an authentic triangular arrangement are H. folkertsi, H. pitymi and H. tualatinensis, which coincidentally also feature a rostral projection of the rostellar capsule. Yet, even in this group, there is considerable variation in the testicular arrangement, as shown by the clearly triangular arrangement of the type specimens of H. folkertsi (Makarikov et al, 2015), which contrast with the almost linear arrangement seen in conspecific specimens identified here (specimen collected from the prairie vole MSB: Mamm: 331573) and documented subsequently (Hoberg et al, 2016).…”

“…Hymenolepis Weinland, 1858 includes species that feature an unarmed scolex with a rudimentary rostellar apparatus, anastomoses connecting ventral excretory canals, saccate uterus and testes arranged triangularly or in a transversal line. There are 10 species known to occur in North America which infect sciurid, arvicoline, geomyid and neotomine rodents (Gardner et al, 2020;Hoberg et al, 2016;Makarikov et al, 2015). In addition, the cosmopolitan H. diminuta Weinland, 1858 has been recorded throughout the continent infecting humans and both synanthropic and wild rodents (Coggins & McDaniel, 1975;Faulkner & Lochmiller, 2000;Harkema, 1946;Harkema & Kartman, 1948;Mollhagan, 1978;Seidenberg et al, 1974).…”

“…Although the majority of Hymenolepis species are known to infect only their definitive host, two species occur in unrelated sympatric mammals. These include H. citelli (McLeod, 1933) and H. folkertsi Makarikov, Nims, Galbreath and Hoberg, 2015; the latter was documented from a variety of unrelated species of cricetid, geomyid, heteromyid and sciurid rodents distributed across the United States (Gardner, 1985;Gardner et al, 2020;Hoberg et al, 2016;Makarikov et al, 2015;Pfaffenberger et al, 1985;Riley & Shannon, 1922;Smith et al, 1953). Recently, the use of mitochondrial genes has assisted in establishing the species identity of individual tapeworms identified as H. folkertsi collected across the vast geography of North America and from a wide diversity of mammals.…”

“…Recently, the use of mitochondrial genes has assisted in establishing the species identity of individual tapeworms identified as H. folkertsi collected across the vast geography of North America and from a wide diversity of mammals. By analyzing sequence divergence, Hoberg et al (2016), established inter-population genetic structure and related this to the characterization of intraspecific morphological variability of diagnostic characters. They also determined that the genetic distance among individuals of H. folkertsi across the distribution of the species oscillates between 1.9 and 2.7% (Hoberg et al, 2016).…”

“…By analyzing sequence divergence, Hoberg et al (2016), established inter-population genetic structure and related this to the characterization of intraspecific morphological variability of diagnostic characters. They also determined that the genetic distance among individuals of H. folkertsi across the distribution of the species oscillates between 1.9 and 2.7% (Hoberg et al, 2016). A similar approach has been used to evaluate the intraspecific genetic diversity in species of the hymenolepidid Arostrilepis Mas-Coma and Tenora, 1997 (Makarikov et al, 2020) and provide identifications for human-dwelling hymenolepidids (Nkouawa et al, 2016).…”