Heterozygote deficiencies in parasite populations: an evaluation of interrelated hypotheses in the raccoon tick, Ixodes texanus

Abstract

Population genetics is increasingly being used to study the biology of parasites at the scales of both the host (infrapopulation, IP) and host population (component population, CP). In this study we tested three mechanistic hypotheses that could explain deviations from Hardy-Weinberg equilibrium (HWE) expectations due to heterozygote deficits (HDs) at the CP scale in raccoon ticks (Ixodes texanus; n ¼ 718) collected from raccoons (Procyon lotor; n ¼ 91) and genotyped at 11 microsatellite loci. These hypotheses were presence of technical issues (for example, null alleles), hierarchical structure (for example, host demography) and cryptic structure (for example, kin structure). Although statistical support for null alleles existed, their presence would also be expected to lead to an underestimation in levels of relatedness, and thus kin structure. However, we found the opposite pattern: significant HD at the IP scale being more likely in CPs with significant vs non-significant levels of kin structure. Our analyses revealed that pooling of kin groups could lead to highly variable levels of F IS among loci, a pattern usually suggestive of null alleles. We used Monte-Carlo (MC) simulations to show that the existence of subdivided breeding groups and high variance in individual reproductive success could adequately explain deviations from HWE in I. texanus. Thus, our results indicate that biological factors can lead to patterns that have usually been interpreted as technical issues (for example, null alleles), and that it is important to take such factors into consideration because loci deviating from HWE likely reflect the effects of real biological processes.

Thirty years of tick population genetics: A comprehensive review

“…A deficit of heterozygotes was observed in Ixodes texanus infrapopulations collected from raccoons (Dharmarajan et al, 2010a). Three hypotheses were proposed to explain this deficit: technical issues, population structure due to the host or tick life stage, and the presence of a cryptic population structure.…”

“…The occurrence of null alleles did not explain the heterozygote deficit entirely (similar to I. ricinus) and further exploration showed the existence of kin structure among samples of I. texanus ticks. This kin structure resulted from breeding group structure among individual raccoon hosts, coupled with a large variance in the reproductive success of adult ticks (Dharmarajan et al, 2010a). Another nidicolous tick, Ixodes arboricola, demonstrates high relatedness among larval groups from individual harborage sites (nest cavities in trees and man-made nest boxes) found in woodlots near Antwerp, Belgium.…”

“…Microsatellites High structure results from nidiculous behavior and kin structure despite a moderately mobile host (raccoon) Dharmarajan et al (2010a) Ixodes uriae Microsatellites, DNA sequence (COIII)…”

Population genetic structure of the tree-hole tick Ixodes arboricola (Acari: Ixodidae) at different spatial scales

“…The fact that significant genetic differentiation was found among nest boxes within woodlots suggests that HDs are caused by subdivision of tick populations among nest boxes within woodlots (Wahlund effect). This is in line with studies of the raccoon tick I. texanus, where highly variable levels of HD among loci and populations were caused by subdivided breeding groups and high variance in individual reproductive success (Dharmarajan et al, 2011). The fact that no HDs have been found within nest boxes supports the claim that tick populations are subdivided within woodlots, although power of this test is low and hence further work is needed to draw more decisive conclusions.…”

“…The current study is the first that investigated spatial genetic structure of a bird-specialised tick in a terrestrial ecosystem, following work on other endophilic ticks (McCoy et al, 2003;Guzinski et al, 2009;Dharmarajan et al, 2011). Because I. arboricola has a low intrinsic mobility (Heylen and Matthysen, 2010) while its main hosts (P. major and C. caeruleus) show high fidelity to cavities (Gosler, 1993), tick populations were expected to be spatially structured among woodlots and among nest boxes within woodlots and ticks within nest boxes to be highly related.…”