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Data for: Direct evidence for increased disease resistance in polyandrous broods exists only in eusocial

Citation

Soper, Deanna; Ekroth, Alice; Martins, M Joao (2021), Data for: Direct evidence for increased disease resistance in polyandrous broods exists only in eusocial, Dryad, Dataset, https://doi.org/10.5061/dryad.dv41ns1zw

Abstract

Background

The ‘genetic diversity’ hypothesis posits that polyandry evolved as a mechanism to increase genetic diversity within broods. One extension of this hypothesis is the ‘genetic diversity for disease resistance’ hypothesis (GDDRH). Originally designed for eusocial Hymenoptera, GDDRH states that polyandry will evolve as an effect of lower parasite prevalence in genetically variable broods. However, this hypothesis has been broadly applied to several other taxa. It is unclear how much empirical evidence supports GDDRH specifically, especially outside eusocial Hymenoptera.

Results

This question was addressed by conducting a literature review and posteriorly conducting meta-analyses on the data available using Hedges’s g. The literature review found 10 direct and 32 indirect studies with both having a strong publication bias towards Hymenoptera.  Two meta-analyses were conducted and both found increased polyandry (direct tests; n = 8, g = 0.2283, p = <0.0001) and genetic diversity generated by other mechanisms (indirect tests; n  = 10, g = 0.21, p = <0.0001) reduced parasite load.  A subsequent moderator analysis revealed that there were no differences among Orders, indicating there may be applicability outside of Hymenoptera.  However, due to publication bias and low sample size we must exercise caution with these results. 

Conclusion

Despite the fact that the GDDRH was developed for Hymenoptera, it is frequently applied to other taxa.  This study highlights the low amount of direct evidence supporting GDDRH, particularly outside of eusocial Hymenoptera.  It calls for future research to address species that have high dispersal rates and contain mixes of solitary and communal nesting.

Methods

For definition purposes, ‘parasites’ will be used to mean all infecting agents, which include microbial pathogens. We used the guidelines Preferred Reporting Items for Systematic reviews and Meta-Analysis (PRISMA) outlined in Moher et al. (2009) to undergo a literature search to glean studies that test the GDDRH both directly and indirectly (see Sup. Fig. 1).  To determine how much direct evidence supporting the GDDRH exists, a literature search was conducted using both Google Scholar and Web of Science. Combinations of the keywords; “Polyandry”, ”Genetic Diversity”, “Multiple Mating”, and ”Disease Resistance” were used for each database in May 2020. Next, citations were removed if replicates were found between searches and databases, as well as non-peer reviewed sources (i.e. books, dissertations). This resulted in 2,106 citations being left. Titles were then evaluated for relevance and 2,018 papers were removed. Of the articles remaining we assessed the following parameters: (1) disease or infection evaluation (2) genetic diversity alterations and (3) determination of study type (reviews were eliminated). Those studies that assessed infection, and altered genetic diversity were further evaluated and parsed into direct and indirect studies. 

This process resulted in 42 studies that were grouped into direct or indirect tests of the GDDRH (Table 1). For the purposes of this paper, a direct study testing GDDRH is defined as one that i) directly measures parasitic infection of offspring, with infection performed either in the field or direct infection in the laboratory, and ii) incorporated correlation with high vs. low genetically diverse host populations through mating strategy differences, i.e. monandry vs. polyandry. Comparing monandrous broods to polyandrous broods are valuable treatments when genetic relatedness is not available: monandry should have lower levels of genetic diversity providing the best alternative to polyandry for comparison. However, one study does not use monandrous broods, but rather compares the relationship between parasite load and varying levels of promiscuity (i.e., 10 to 28 mated males per queen in Neumann & Moritz, 2000, with genetic relatedness reported). Another study manipulated male genetic diversity that led to the effective mating rate being 1.3 versus 4 males (Baer & Schmid-Hempel, 1999). Both studies were classified as direct tests of the GDDRH. Indirect studies examine parasitic infection in groups that may have different levels of genetic diversity generated through other mechanisms. For example, genetic diversity was manipulated through groups founded by one (monogyne) or more than one female (polygyne). Although that is a mechanism for increasing genetic diversity, it does not address polyandrous behavior, and as a result those studies were classified as indirect as long as infection was also assessed.

We then assessed the studies to determine if they could be included in the meta-analysis based on the following parameters: (i) a comparison between high and low genetic diversity groups and (ii) assess parasite success (i.e., mortality).  We excluded studies that used heterogeneity as a measure for genetic diversity as we were interested in the benefits of polyandry at the population level and not individual level on parasite success.  We also excluded studies that were mathematical models and meta-analyses.  This left 8 direct studies and 10 indirect studies that we gleaned data from to conduct our meta-analysis.

We conducted a meta-analysis following the methods described in Hedges (1981), using Hedges’s g to estimate effect sizes. Standard mean difference was calculated using the escalc function in the package metafor in R v. 1.3.1056 (R Development Core Team). The web-based tool WebPlotDigitizer (https://automeris.io/WebPlotDigitizer/userManual.pdf) was used to extract data from publication plots when raw data was not available.

The terms of the GDDRH posit that polyandry is favored when it results in increased genetic diversity, gambling in the likelihood that half-siblings will vary in resilience to parasites. In the direct studies dataset, standard mean difference effect sizes were calculated by extracting parasite harm mean measurements and their standard deviations in two groups: monandry or low polyandry and high polyandry. In one study (Tarpy & Seeley 2006), t-values and degrees of freedom were extracted due to the lack of means and standard deviations. As most direct studies looked at the effects of GDDRH in Hymenoptera, we first performed a nested random mixed effects model using the rma.mv function to account for phylogenetic non-independence. The same method to obtain standard mean difference was applied on studies indirectly testing GDDRH; however, here, groups were categorized into low genetic diversity and high genetic diversity.

Additionally, we tested whether the magnitude of the relationship was dependent on eusocial Hymenoptera for both datasets by performing a third analysis using “host Order” as a moderator variable.

Last, we tested for a potential publication bias by plotting a funnel plot for both datasets, i.e., direct and indirect studies.