Isolation of Novel Trypanosomatid, Zelonia australiensis sp. nov. (Kinetoplastida: Trypanosomatidae) Provides Support for a Gondwanan Origin of Dixenous Parasitism in the Leishmaniinae
Abstract:The genus Leishmania includes approximately 53 species, 20 of which cause human leishmaniais; a significant albeit neglected tropical disease. Leishmaniasis has afflicted humans for millennia, but how ancient is Leishmania and where did it arise? These questions have been hotly debated for decades and several theories have been proposed. One theory suggests Leishmania originated in the Palearctic, and dispersed to the New World via the Bering land bridge. Others propose that Leishmania evolved in the Neotropic… Show more
“…Alternatively, age estimates from fossils could be an option, but nematode fossils are rare and their correct placement in the phylogeny can be challenging. Biogeographic events are another possibility (i.e., Barratt et al., ) and have been used for host divergence time estimates. However, they were found unsuitable in our study due to the time intervals between island formation and host colonization.…”
Episodes of expansion and isolation in geographic range over space and time, during which parasites have the opportunity to expand their host range, are linked to the development of host-parasite mosaic assemblages and parasite diversification. In this study, we investigated whether island colonization events lead to host range oscillations in a taxon of host-specific parasitic nematodes of the genus Spauligodon in the Canary Islands. We further investigated whether range oscillations also resulted in shifts in host breadth (i.e., specialization), as expected for parasites on islands. Parasite phylogeny and divergence time estimates were inferred from molecular data with Bayesian methods. Host divergence times were set as calibration priors after a priori evaluation with a global-fit method of which individual host-parasite associations likely represent cospeciation links. Parasite colonization history was reconstructed, followed by an estimation of oscillation events and specificity level. The results indicate the presence of four Spauligodon clades in the Canary Islands, which originated from at least three different colonization events. We found evidence of host range oscillations to truly novel hosts, which in one case led to higher diversification. Contemporary host-parasite associations show strong host specificity, suggesting that changes in host breadth were limited to the shift period. Lineages with more frequent and wider taxonomic host range oscillations prior to the initial colonization event showed wider range oscillations during colonization and diversification within the archipelago. Our results suggest that a lineage's evolutionary past may be the best indicator of a parasite's potential for future range expansions.
“…Alternatively, age estimates from fossils could be an option, but nematode fossils are rare and their correct placement in the phylogeny can be challenging. Biogeographic events are another possibility (i.e., Barratt et al., ) and have been used for host divergence time estimates. However, they were found unsuitable in our study due to the time intervals between island formation and host colonization.…”
Episodes of expansion and isolation in geographic range over space and time, during which parasites have the opportunity to expand their host range, are linked to the development of host-parasite mosaic assemblages and parasite diversification. In this study, we investigated whether island colonization events lead to host range oscillations in a taxon of host-specific parasitic nematodes of the genus Spauligodon in the Canary Islands. We further investigated whether range oscillations also resulted in shifts in host breadth (i.e., specialization), as expected for parasites on islands. Parasite phylogeny and divergence time estimates were inferred from molecular data with Bayesian methods. Host divergence times were set as calibration priors after a priori evaluation with a global-fit method of which individual host-parasite associations likely represent cospeciation links. Parasite colonization history was reconstructed, followed by an estimation of oscillation events and specificity level. The results indicate the presence of four Spauligodon clades in the Canary Islands, which originated from at least three different colonization events. We found evidence of host range oscillations to truly novel hosts, which in one case led to higher diversification. Contemporary host-parasite associations show strong host specificity, suggesting that changes in host breadth were limited to the shift period. Lineages with more frequent and wider taxonomic host range oscillations prior to the initial colonization event showed wider range oscillations during colonization and diversification within the archipelago. Our results suggest that a lineage's evolutionary past may be the best indicator of a parasite's potential for future range expansions.
“…Few autochthonous CL cases, previously attributed to ‘ Leishmania siamensis ’, were reported in Germany (in horses ) and in Texas (in one Morgan horse ). After taxonomic revision of the genus Leishmania subgenus Mundinia , the species Leishmania ( Mundinia ) martiniquensis is considered the aetiological agent; the name of ‘ L. siamensis ’ ( nomen nudum ) being taxonomically invalid .…”
Section: Leishmania Spp In Infected Equids Of the New And Old Worldsmentioning
Summary
Infection of equids by Leishmania (L.) parasites was previously described in both the Old and New World, particularly in Central and South America. Equine cutaneous leishmaniasis (CL) is caused by the Leishmania species, L. Viannia (V.) braziliensis and L. infantum, previously identified in humans and other parasite hosts living in the same geographic endemic areas. Sporadic autochthonous clinical cases, with no travel history, were documented in several countries including Germany, Portugal, Spain, Texas and Brazil; L. infantum and L. (Mundinia) martiniquensis were the infectious species. Prevalence of subclinical infections is extremely low and CL is observed in only a small proportion of infected animals with the appearance of single or multiple cutaneous lesions located on the head, external ear, scrotum, legs and the neck. To date, there has been no report of visceral abnormalities. However, the mild clinical profile of the disease and its spontaneous regression may indicate that skin lesions related to Leishmania infection is underdiagnosed. Importantly, although the prevalence of Leishmania infections in the equine population is low, a risk may rise from its potential involvement in the parasite transmission cycles as a source of infection for phlebotomine vectors and susceptible mammalian hosts. This review article summarises our current knowledge of the epidemiology, clinical presentation and diagnosis of Leishmania‐infected equids.
“…Debate over which section was the more primitive ensued to decide which section should occupy the root of phylogenetic trees with the Hypopylaric (subgenus Sauroleishmania ) and Peripylaric (subgenus Viannia ) species representing the prime contenders [66, 67]. Phylogenetic evidence indicates that Hypopylaria does not reflect the most primitive state as saurian species occupy a position closer to the crown of trees than Viannia [68]. In fact, the subgenus Mundinia is the most basal subgenus of Leishmania [28, 68], though knowledge on the development of Mundina in invertebrates is limited.Fig.…”
Section: Development In Invertebratesmentioning
confidence: 99%
“…Phylogenetic evidence indicates that Hypopylaria does not reflect the most primitive state as saurian species occupy a position closer to the crown of trees than Viannia [68]. In fact, the subgenus Mundinia is the most basal subgenus of Leishmania [28, 68], though knowledge on the development of Mundina in invertebrates is limited.Fig. 6Diagrammatic representation of the three Leishmania sections proposed by Lainson & Shaw (1979).…”
Section: Development In Invertebratesmentioning
confidence: 99%
“…These and other subtleties once served as taxon-defining characteristics under the classic system, and are now considered to a very minor extent given the inadequacies of this system revealed by genetics [26, 68, 97]. Phylogenetic analyses have culminated in the renaming of several species due to various instances of polyphyly introduced by the classic system, and are now considered mandatory for making accurate taxonomic assignments for new isolates [27, 28, 97, 99, 100].…”
Trypanosomatids are protozoan parasites of the class Kinetoplastida predominately restricted to invertebrate hosts (i.e. possess a monoxenous life-cycle). However, several genera are pathogenic to humans, animals and plants, and have an invertebrate vector that facilitates their transmission (i.e. possess a dixenous life-cycle). Phytomonas is one dixenous genus that includes several plant pathogens transmitted by phytophagous insects. Trypanosoma and Leishmania are dixenous genera that infect vertebrates, including humans, and are transmitted by hematophagous invertebrates. Traditionally, monoxenous trypanosomatids such as Leptomonas were distinguished from morphologically similar dixenous species based on their restriction to an invertebrate host. Nonetheless, this criterion is somewhat flawed as exemplified by Leptomonas seymouri which reportedly infects vertebrates opportunistically. Similarly, Novymonas and Zelonia are presumably monoxenous genera yet sit comfortably in the dixenous clade occupied by Leishmania. The isolation of Leishmania macropodum from a biting midge (Forcipomyia spp.) rather than a phlebotomine sand fly calls into question the exclusivity of the Leishmania-sand fly relationship, and its suitability for defining the Leishmania genus. It is now accepted that classic genus-defining characteristics based on parasite morphology and host range are insufficient to form the sole basis of trypanosomatid taxonomy as this has led to several instances of paraphyly. While improvements have been made, resolution of evolutionary relationships within the Trypanosomatidae is confounded by our incomplete knowledge of its true diversity. The known trypanosomatids probably represent a fraction of those that exist and isolation of new species will help resolve relationships in this group with greater accuracy. This review incites a dialogue on how our understanding of the relationships between certain trypanosomatids has shifted, and discusses new knowledge that informs the present taxonomy of these important parasites.
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