Host body size, not host population size, predicts genome-wide effective population size of parasites

Abstract The effective population size (Ne) of an organism is expected to be generally proportional to the total number of individuals in a population. In parasites, we might expect the effective population size to be proportional to host population size and host body size, because both are expected to increase the number of parasite individuals. However, among other factors, parasite populations are sometimes so extremely subdivided that high levels of inbreeding may distort these predicted relationships. Here, we used whole-genome sequence data from dove parasites (71 feather louse species of the genus Columbicola) and phylogenetic comparative methods to study the relationship between parasite effective population size and host population size and body size. We found that parasite effective population size is largely explained by host body size but not host population size. These results suggest the potential local population size (infrapopulation or deme size) is more predictive of the long-term effective population size of parasites than is the total number of potential parasite infrapopulations (i.e., host individuals).


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Parasites, among Earth's most diverse, threatened, and under-protected animals, play a central 17 role in ecosystem function. The effective population size (Ne) of an organism has a profound 18 impact on evolutionary processes, such as the relative contributions of selection and genetic drift 19 to genomic change. Population size is also one of the most important parameters in conservation 20 biology. For free-living organisms, it is expected that Ne is generally proportional to the total 21 number of individuals in a population. However, for parasites, among other factors, populations 22 are sometimes so extremely subdivided that high levels of inbreeding may distort these 23 relationships. In this study, we used whole-genome sequence data from dove parasites and The effective population size (Ne) of an organism has a profound impact on evolutionary 34 processes, such as the relative contributions of selection and genetic drift to genomic change 35 (Wright, 1943;Waples, 2002;Charlesworth, 2009). For free-living organisms, it is generally 36 expected that Ne is proportional to the total number of individuals in a population (census 37 population size, Nc) (Frankham, 1995;Waples, 2002). While population size estimates can often 38 be readily obtained for free-living species, estimating the population size of parasites can be more

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The relationship between long-term effective population size (Ne) and the total number of 42 individuals in a population (Nc) is complex and depends on various ecological and demographic 43 factors (Buffalo, 2021;Charlesworth & Jensen, 2022). According to neutral theory, genetic 44 diversity is expected to increase with population size (Kimura, 1971). However, the observed

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Typically, we might expect that the size of a parasite population is proportional to that of 63 the host, because parasites rely on their hosts for survival and reproduction (Poulin, 2007;Barrett 64 et al., 2008;Clayton et al., 2015). However, population subdivision can also influence measures 65 of Ne for a species (Wright, 1943;Charlesworth et al., 2003). For example, theoretical 66 expectations, based on the island model of population structure, generally predict that subdivided 67 populations have a higher overall long-term Ne than non-subdivided ones (Charlesworth et

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Host body size has been shown to strongly impact infrapopulation size, with larger-88 bodied hosts harboring larger parasite infrapopulations (Poulin, 1999 (Table S1), which 114 are feather lice (Insecta: Ischnocera) of pigeons and doves. We also included five feather louse 115 outgroup taxa for the phylogenomic analyses, selected based on recent higher level 116 phylogenomic studies of feather lice (Table S1). We obtained host body size (body mass)  Table S1 for details). For the newly sequenced samples, which had been stored in 95%

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We prepared genomic libraries using the Hyper library construction kit (Kapa Biosystems). We

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We trimmed adapters and demultiplexed the sequencing data using bcl2fastq v.2.20 to generate 142 final fastq files. We deposited raw reads for each library in NCBI SRA (Table S1).

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Single-copy orthologs assembly   gene, we subsampled four million reads (two million read1 and two million read2) from each 160 library using Seqtk v1.3 (Li, 2022). As the reference target for constructing COI sequences from 161 all samples in our current work, we used a COI sequence from Columbicola columbae that had 162 previously been published (Johnson et al., 2007). For these assemblies, we ran aTRAM for only a 163 single iteration. Then, we translated COI DNA sequences to amino acids, aligned them, and 164 threaded the DNA back through the aligned proteins to obtain nucleotide data. As a quality 165 control procedure, we blasted COI sequences against NCBI to identify any identical or nearly 7 identical to previously generated Sanger sequences. We estimated a phylogenetic tree based on  HostPopulationSize. For each of these formulas, we tried both corPagel and corBrownian 258 correlation structures, resulting in a total of six models. CorPagel accounts for a variable rate of 259 phylogenetic signal (Pagel, 1999;Freckleton et al., 2002), whereas corBrownian assumes a 260 constant rate of trait evolution along the branches of the phylogenetic tree (Felsenstein, 1985; 261 Martins & Hansen, 1997). We checked models via visual inspection of diagnostic plots (residuals 262 vs. fitted values and QQ plots to check normality).

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Out of the initial 94 samples, 18 were excluded from further analyses because they had 267 mitochondrial COI genetic distances less than 5% in the species delimitation analysis. The same 268 result was on inspection of the COI tree, in which these 18 samples were grouped with the 269 retained species with zero or almost zero branch length, indicating that they likely represent the  Specifically, we identified 36 cospeciation events, 7 of which occurred between terminal sister 277 species and were used to generate the dated ultrametric tree for the PGLS analysis.

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Another factor to consider is that smaller-bodied host species also typically have a lower parasite 328 prevalence (i.e., proportion of host individuals that are inhabited by the parasite) (Bush et al., 329 1997). This pattern might be due to smaller infrapopulations being more susceptible to local 330 extinction because of environmental and demographic stochasticity, a known factor shaping Ne 331 (Charlesworth, 2009;. Therefore, host body size could influence local 10 extinction probability of parasites and thus play a role in determining long-term Ne of permanent 333 parasites (Farrell et al., 2021). Given the lower prevalence and intensity of lice on small-bodied 334 hosts, it may be that the total number of lice in the global population is considerably smaller than

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Another factor to consider is the low among-deme migration rates of permanent parasites. A low 347 migration rate among parasite infrapopulations is expected to increase long-term Ne because of

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In our analysis, we also did not account for the potential effects of selection or demography 360 separately, and assumed that these factors are largely similar across species, allowing us to 361 make meaningful comparisons. However, selection is also known to influence effective population

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Under the global parasite conservation plan, risk assessment, along with applying conservation 382 genomics to parasites, were identified as two of the major goals for parasite conservation over 383 the next decade (Carlson et al., 2020). Our result that host body size, but not host population 384 size, is a good predictor of parasite Ne can easily translate into parasite conservation practices, 385 drawing attention to conservation of smaller bodied hosts as a practice to conserve parasites.

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Overall, our study shows that host body size plays a major role in shaping parasite population 388 genomics and provides evidence for the essential role that individual hosts play as habitat for    Host body size (g) θ R 2 pred = 0.48, p < 0.001