Heterozygosity and fitness in a threatened songbird: blood parasite infection is explained by single-locus but not genome-wide effects

Abstract

In non-pedigreed populations, insights into effects of inbreeding can be obtained by correlations between individual heterozygosity and fitness-related traits (HFCs). Using an information-theoretic approach, we explored whether heterozygosity of microsatellite markers, measured as internal relatedness (IR), is associated with infection by blood parasites (Plasmodium, Trypanosoma, or Leucocytozoon) in the threatened Aquatic Warbler (Acrocephalus paludicola). We also explored whether any of the markers is more influential than others, or than IR, in explaining blood parasitism (single-locus effects). While we observed that IR was a relatively important predictor of Plasmodium parasitism, we did not find strong evidence for IR to correlate with infection by the identified blood parasites, accounting for sex and population effects. Therefore, our data did not support negative inbreeding effects on blood parasite infection in the Aquatic Warbler. However, we found singlelocus effects, such that individuals heterozygous at AW-03 and Ase19 had lower probability of infection by blood parasites pooled together and by Plasmodium, respectively. This indicates that these two markers are in linkage disequilibrium with unknown fitness loci which are related to resisting or clearing blood parasites, and which confer a heterozygote advantage in the Aquatic Warbler. Our results add to the growing evidence that single-locus effects contribute more to HFCs than formerly recognized and have implications for Aquatic Warbler conservation. Keywords Heterozygosity-fitness correlations • General effects • Local effects • Plasmodium • Trypanosoma • Aquatic Warbler Zusammenfassung Heterozygosität und Fitness bei einem bedrohten Singvogel: Blutparasitenbefall wird durch Einzel-Lokus, aber nicht durch Genom-weite Effekte erklärt Für Populationen, für die keine Informationen zu Abstammungsverhältnissen vorliegen, können Einblicke über Inzuchteffekte durch Korrelationen zwischen individueller Heterozygosität und dem Auftreten Fitness-relevanter Merkmale ("heterozygosity-fitness-correlations"; HFCs) gewonnen werden. Für den bedrohten Seggenrohrsänger (Acrocephalus paludicola) untersuchten wir, ob Heterozygosität in Mikrosatelliten Markern, gemessen als interne Verwandtschaft ("internal relatedness"; IR), mit der Befall durch Blutparasiten (Plasmodium, Trypanosoma oder Leucocytozoon) korreliert, in dem wir einen Informationstheoretischen Ansatz wählten. Wir untersuchten ebenfalls, ob irgendeiner der Marker einen größeren Einfluss hat als andere Marker, oder als IR, um den Befall mit Blutparasiten zu erklären (Einzel-Lokus Effekt). Während wir beobachteten, dass IR ein relativ wichtiger Prädiktor für Parasitenbefall mit Plasmodium ist, fanden wir keinen Communicated by M. Wink.

Low genetic diversity and high gene flow in the Aquatic Warbler (Acrocephalus paludicola), a threatened marshland songbird with a fragmented breeding range

“…Seventeen microsatellite loci were PCR‐amplified according to the protocols described in Kubacka et al . (2020) (contemporary samples) and Salewski et al . (2012) (historical samples).…”

“…DNA extractions were performed using either phenol-chloroform or ammonium acetate precipitation protocols (Bruford et al 1998, Sambrook & Russell 2001. Seventeen microsatellite loci were PCR-amplified according to the protocols described in Kubacka et al (2020) (contemporary samples) and Salewski et al (2012) (historical samples). Two historical samples were PCRamplified together with the contemporary ones for 11 of the 17 markers (not all markers were used due to limitations resulting from processing the samples in three different projects), to serve as controls for possible length shifts.…”

Genomic heterozygosity is associated with parasite abundance, but the effects are not mediated by host condition

“…However, our individual-scale analyses, which had lower power due to sample size, found no relationship between heterozygosity and infection status. Previous studies from diverse systems often (Acevedo-Whitehouse et al 2005 , 2006 ; Townsend et al 2018 ; Banks et al 2020 ; DeCandia et al 2021 ), but not always (Acevedo-Whitehouse et al 2009 ; Townsend et al 2018 ; Kubacka et al 2020 ; Martin et al 2021 ), find negative associations between genome-wide variation and infection status (reviewed in (Blanchong et al 2016 )). While there is well-described functional genetic variation for host susceptibility to coccidia infection (Klesius and Hinds 1979 ; Kim et al 2006 ; Boulton et al 2018 ; present study) reviewed in (Chapman et al 2013 )), here we also document a role for genome-wide neutral diversity.…”