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Rapid host expansion of an introduced parasite, the spiny rat louse Polyplax spinulosa (Psocodea: Phthiraptera: Polyplacidae), among endemic rodents in Australia.

ABSTRACT: BACKGROUND:Historical European exploration and colonization resulted in the introduction of four species of rodents to the Australian continent from Eurasia: the brown rat, Rattus norvegicus, the black rat, R. rattus, the Pacific rat, R. exulans, and the house mouse, Mus musculus. The spread of these rodents created opportunities for their co-introduced sucking lice to parasitize and adapt to endemic rodents in Australia. METHODS:We collected sucking lice from rodent specimens in seven museums across Australia. We identified the spiny rat louse, Polyplax spinulosa, based on morphology. We sequenced the mitochondrial cox1 and rrnL genes of P. spinulosa specimens and constructed a phylogenetic tree with rrnL sequences. RESULTS:We examined 989 rodent specimens of 54 species and collected 2111 adult sucking lice and 1064 nymphal sucking lice. We found that P. spinulosa had nearly doubled its host range by parasitizing at least six endemic rodent species in Australia. The other two introduced lice, P. serrata and Hoplopleura pacifica, however, have apparently failed to expand to any endemic rodents in Australia. Our analysis of mitochondrial rrnL gene sequences divided P. spinulosa into two genotypes (European vs Southeast Asian), which differ by 7.5%; both genotypes were introduced into Australia and then expanded their host ranges to include endemic rodents. CONCLUSIONS:The earliest record of a European ship landing in Australia was in 1606, followed by British settlement in 1788. The expansion of P. spinulosa to at least six endemic rodent species in Australia has therefore occurred in the time frame of 200 to 400 years, which is extremely rapid relative to its host expansion to eight native rat species in Eurasia in ~?16 million years since it diverged from P. serrata. The host expansion of P. spinulosa is remarkable for a blood-sucking louse and is in stark contrast to the absence of host expansion by P. serrata and H. pacifica. Comparison among these three introduced sucking lice indicated that both louse-specific factors and host-specific factors can contribute to the success or failure of host expansion.

SUBMITTER: Wang W

PROVIDER: S-EPMC7029564 | biostudies-literature | 2020 Feb

REPOSITORIES: biostudies-literature

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Rapid host expansion of an introduced parasite, the spiny rat louse Polyplax spinulosa (Psocodea: Phthiraptera: Polyplacidae), among endemic rodents in Australia.

Wang Wei W Durden Lance A LA Shao Renfu R

Parasites & vectors 20200218 1

<h4>Background</h4>Historical European exploration and colonization resulted in the introduction of four species of rodents to the Australian continent from Eurasia: the brown rat, Rattus norvegicus, the black rat, R. rattus, the Pacific rat, R. exulans, and the house mouse, Mus musculus. The spread of these rodents created opportunities for their co-introduced sucking lice to parasitize and adapt to endemic rodents in Australia.<h4>Methods</h4>We collected sucking lice from rodent specimens in ...[more]

PMID: 32070404

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Project description:UnlabelledRoughly 10% to 15% of insect species host heritable symbiotic bacteria known as endosymbionts. The lice parasitizing mammals rely on endosymbionts to provide essential vitamins absent in their blood meals. Here, we describe two bacterial associates from a louse, Proechinophthirus fluctus, which is an obligate ectoparasite of a marine mammal. One of these is a heritable endosymbiont that is not closely related to endosymbionts of other mammalian lice. Rather, it is more closely related to endosymbionts of the genus Sodalis associated with spittlebugs and feather-chewing bird lice. Localization and vertical transmission of this endosymbiont are also more similar to those of bird lice than to those of other mammalian lice. The endosymbiont genome appears to be degrading in symbiosis; however, it is considerably larger than the genomes of other mammalian louse endosymbionts. These patterns suggest the possibility that this Sodalis endosymbiont might be recently acquired, replacing a now-extinct, ancient endosymbiont. From the same lice, we also identified an abundant bacterium belonging to the genus Rickettsia that is closely related to Rickettsia ricketsii, a human pathogen vectored by ticks. No obvious masses of the Rickettsia bacterium were observed in louse tissues, nor did we find any evidence of vertical transmission, so the nature of its association remains unclear.ImportanceMany insects are host to heritable symbiotic bacteria. These heritable bacteria have been identified from numerous species of parasitic lice. It appears that novel symbioses have formed between lice and bacteria many times, with new bacterial symbionts potentially replacing existing ones. However, little was known about the symbionts of lice parasitizing marine mammals. Here, we identified a heritable bacterial symbiont in lice parasitizing northern fur seals. This bacterial symbiont appears to have been recently acquired by the lice. The findings reported here provide insights into how new symbioses form and how this lifestyle is shaping the symbiont genome.

Project description:The evolution of pest resistance to management strategies is a major challenge for farmed systems. Mitigating the effects of pest adaptation requires identifying the selective pressures imposed by these strategies. In Atlantic salmon (Salmo salar) aquaculture, barriers are used to prevent salmon louse (Lepeophtheirus salmonis) larvae (copepodids) from entering salmon cages. These barriers are effective against shallow-swimming copepodids, but those swimming deeper can pass underneath and infest salmon. Laboratory experiments suggest that depth regulation in copepodids is a variable behavioural trait with a genetic basis. We used biological-hydrodynamic dispersal models to assess how this trait variation alters the dispersion of lice through the ocean environment and into farms. The dispersal of copepodids with 3 behavioural phenotypes (deep, mean or shallow) was modelled over winter-spring and spring-summer periods in a Norwegian fjord system with intensive aquaculture. The infestation pressure of each phenotype on barrier cages was estimated from their modelled depth distributions: copepodids deeper than 10 m were predicted to successfully pass underneath barriers. The deep phenotype was the most abundant below 10 m and reached infestation pressures 3 times higher than that of the mean phenotype. In contrast, the shallow phenotype infestation pressure reached less than half that of the mean phenotype. These differences in relative fitness indicate that barriers can impose strong directional selection on the swimming behaviour of copepodids. The strength of this selection varied seasonally and geographically, with selection for the deep phenotype stronger in winter-spring and at coastal locations than in spring-summer and within fjords. These findings can be applied across farms to slow louse adaptation, by limiting barriers during situations of strong selection, although this must be balanced against trade-offs to short-term efficacy. More broadly, our study highlights new ways in which dispersal models can address evolutionary questions crucial for sustainable parasite management in aquaculture.

Dataset Information

Rapid host expansion of an introduced parasite, the spiny rat louse Polyplax spinulosa (Psocodea: Phthiraptera: Polyplacidae), among endemic rodents in Australia.

Publications

Rapid host expansion of an introduced parasite, the spiny rat louse Polyplax spinulosa (Psocodea: Phthiraptera: Polyplacidae), among endemic rodents in Australia.

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