Marc J. Lajeunesse

Host range and local parasite adaptation

Parasites may be expected to become locally adapted to their hosts. However, while many empirical studies have demonstrated local parasite adaptation, others have failed to demonstrate it, or have shown local parasite maladaptation. Researchers have suggested that gene flow can swamp local parasite–host dynamics and produce local adaptation only at certain geographical scales; others have argued that evolutionary lags can account for both null and maladaptive results. In this paper, we use item response theory (IRT) to test whether host range influences the likelihood of parasites locally adapting to their hosts. We collated 32 independent experiments testing for local adaptation, where parasites could be assigned as having either broad or narrow host ranges (BHR and NHR, respectively). Twenty‐five tests based on BHR parasites had a significantly lower average effect size than seven NHR tests, indicating that studies based on BHR parasites are less likely to demonstrate local parasite adaptation. We argue that this may relate to evolutionary lags during diffuse coevolution of BHR parasites with their hosts, rather than differences in experimental approaches or other confounds between BHR and NHR studies.

Meta-Analysis and the Comparative Phylogenetic Method

Meta‐analysis has contributed substantially to shifting paradigms in ecology and has become the primary method for quantitatively synthesizing published research. However, an emerging challenge is the lack of a statistical protocol to synthesize studies and evaluate sources of bias while simultaneously accounting for phylogenetic nonindependence of taxa. Phylogenetic nonindependence arises from homology, the similarity of taxa due to shared ancestry, and treating related taxa as independent data violates assumptions of statistics. Given that an explicit goal of meta‐analysis is to generalize research across a broad range of taxa, then phylogenetic nonindependence may threaten conclusions drawn from such reviews. Here I outline a statistical framework that integrates phylogenetic information into conventional meta‐analysis when (a) taking a weighted average of effect sizes using fixed‐ and random‐effects models and (b) testing for homogeneity of variances. I also outline how to test evolutionary hypotheses with meta‐analysis by describing a method that evaluates phylogenetic conservatism and a model‐selection framework that competes neutral and adaptive hypotheses to explain variation in meta‐analytical data. Finally, I address several theoretical and practical issues relating to the application and availability of phylogenetic information for meta‐analysis.

On the meta-analysis of response ratios for studies with correlated and multi-group designs

A common effect size metric used to quantify the outcome of experiments for ecological meta-analysis is the response ratio (RR): the log proportional change in the means of a treatment and control group. Estimates of the variance of RR are also important for meta-analysis because they serve as weights when effect sizes are averaged and compared. The variance of an effect size is typically a function of sampling error; however, it can also be influenced by study design. Here, I derive new variances and covariances for RR for several often-encountered experimental designs: when the treatment and control means are correlated; when multiple treatments have a common control; when means are based on repeated measures; and when the study has a correlated factorial design, or is multivariate. These developments are useful for improving the quality of data extracted from studies for meta-analysis and help address some of the common challenges meta-analysts face when quantifying a diversity of experimental designs with the response ratio.

Does phylogeny matter? Assessing the impact of phylogenetic information in ecological meta‐analysis

Meta-analysis is increasingly used in ecology and evolutionary biology. Yet, in these fields this technique has an important limitation: phylogenetic non-independence exists among taxa, violating the statistical assumptions underlying traditional meta-analytic models. Recently, meta-analytical techniques incorporating phylogenetic information have been developed to address this issue. However, no syntheses have evaluated how often including phylogenetic information changes meta-analytic results. To address this gap, we built phylogenies for and re-analysed 30 published meta-analyses, comparing results for traditional vs. phylogenetic approaches and assessing which characteristics of phylogenies best explained changes in meta-analytic results and relative model fit. Accounting for phylogeny significantly changed estimates of the overall pooled effect size in 47% of datasets for fixed-effects analyses and 7% of datasets for random-effects analyses. Accounting for phylogeny also changed whether those effect sizes were significantly different from zero in 23 and 40% of our datasets (for fixed- and random-effects models, respectively). Across datasets, decreases in pooled effect size magnitudes after incorporating phylogenetic information were associated with larger phylogenies and those with stronger phylogenetic signal. We conclude that incorporating phylogenetic information in ecological meta-analyses is important, and we provide practical recommendations for doing so.

Evolution of latex and its constituent defensive chemistry in milkweeds (Asclepias): a phylogenetic test of plant defense escalation

A tremendous diversity of plants exude sticky and toxic latex upon tissue damage, and its production has been widely studied as a defensive adaptation against insect herbivores. Here, we address variation in latex production and its constituent chemical properties (cardenolides and cysteine proteases) in 53 milkweeds [Asclepias spp. (Apocynaceae)], employing a phylogenetic approach to test macroevolutionary hypotheses of defense evolution. Species were highly variable for all three traits, and they showed little evidence for strong phylogenetic conservatism. Latex production and the constituent chemical defenses are thus evolutionarily labile and may evolve rapidly. Nonetheless, in phylogenetically independent analyses, we show that the three traits show some correlations (and thus share a correlated evolutionary history), including a positive correlation between latex exudation and cysteine protease activity. Conversely, latex exudation and cysteine protease activity both showed a trade‐off with cardenolide concentrations in latex. We also tested whether these traits have increased in their phenotypic values as the milkweeds diversified, as predicted by plant defense escalation theory. Alternative methods of testing this prediction gave conflicting results – there was an overall negative correlation between amount of evolutionary change and amount of latex exudation; however, ancestral state reconstructions indicated that most speciation events were associated with increases in latex. We conclude by (i) summarizing the evidence of milkweed latex itself as a multivariate defense including the amount exuded and toxin concentrations within, (ii) assessing the coordinated evolution of latex traits and how this fits with our previous notion of ‘plant defense syndromes’, and finally, (iii) proposing a novel hypothesis that includes an ‘evolving community of herbivores’ that may promote the escalation or decline of particular defensive strategies as plant lineages diversify.

Sex differences in mercury contamination of birds: testing multiple hypotheses with meta-analysis.

The sex of a bird can, in principle, affect exposure and accumulation of mercury. One conventional explanation for sex differences in mercury burden suggests female birds should have lower concentrations than conspecific males, because breeding females can depurate methylmercury to their eggs. However, sex differences in body burden of mercury among birds are not consistent. We used meta-analysis to synthesize 123 male-female comparisons of mercury burden from 50 studies. For breeding birds, males had higher concentrations of mercury than did females, supporting egg depuration as a mechanism. However, the percentage of female body mass represented by a clutch did not significantly predict the magnitude of the sex difference in mercury contamination, as predicted. Furthermore, whether species were semialtrical or altrical versus semiprecocial or precocial also did not explain sex differences in mercury burden. Foraging guild of a species did explain near significant variation in sex differences in mercury burden where piscivores and invertivores showed significant sex differences, but sex differences were not detected for carnivores, herbivores, insectivores, and omnivores. The magnitude and direction of sexual size dimorphism did not explain variation in sex differences in mercury burden among breeding birds. We reveal targeted research directions on mechanisms for sex differences in mercury and confirm that sex is important to consider for environmental risk assessments based on breeding birds.

Home-field advantage? evidence of local adaptation among plants, soil, and arbuscular mycorrhizal fungi through meta-analysis

BackgroundLocal adaptation, the differential success of genotypes in their native versus foreign environment, arises from various evolutionary processes, but the importance of concurrent abiotic and biotic factors as drivers of local adaptation has only recently been investigated. Local adaptation to biotic interactions may be particularly important for plants, as they associate with microbial symbionts that can significantly affect their fitness and may enable rapid evolution. The arbuscular mycorrhizal (AM) symbiosis is ideal for investigations of local adaptation because it is globally widespread among most plant taxa and can significantly affect plant growth and fitness. Using meta-analysis on 1170 studies (from 139 papers), we investigated the potential for local adaptation to shape plant growth responses to arbuscular mycorrhizal inoculation.ResultsThe magnitude and direction for mean effect size of mycorrhizal inoculation on host biomass depended on the geographic origin of the soil and symbiotic partners. Sympatric combinations of plants, AM fungi, and soil yielded large increases in host biomass compared to when all three components were allopatric. The origin of either the fungi or the plant relative to the soil was important for explaining the effect of AM inoculation on plant biomass. If plant and soil were sympatric but allopatric to the fungus, the positive effect of AM inoculation was much greater than when all three components were allopatric, suggesting potential local adaptation of the plant to the soil; however, if fungus and soil were sympatric (but allopatric to the plant) the effect of AM inoculation was indistinct from that of any allopatric combinations, indicating maladaptation of the fungus to the soil.ConclusionsThis study underscores the potential to detect local adaptation for mycorrhizal relationships across a broad swath of the literature. Geographic origin of plants relative to the origin of AM fungal communities and soil is important for describing the effect of mycorrhizal inoculation on plant biomass, suggesting that local adaptation represents a powerful factor for the establishment of novel combinations of fungi, plants, and soils. These results highlight the need for subsequent investigations of local adaptation in the mycorrhizal symbiosis and emphasize the importance of routinely considering the origin of plant, soil, and fungal components.

A cross-biome synthesis of soil respiration and its determinants under simulated precipitation changes

Soil respiration (Rs) is the second-largest terrestrial carbon (C) flux. Although Rs has been extensively studied across a broad range of biomes, there is surprisingly little consensus on how the spatiotemporal patterns of Rs will be altered in a warming climate with changing precipitation regimes. Here, we present a global synthesis Rs data from studies that have manipulated precipitation in the field by collating studies from 113 increased precipitation treatments, 91 decreased precipitation treatments, and 14 prolonged drought treatments. Our meta-analysis indicated that when the increased precipitation treatments were normalized to 28% above the ambient level, the soil moisture, Rs, and the temperature sensitivity (Q10) values increased by an average of 17%, 16%, and 6%, respectively, and the soil temperature decreased by -1.3%. The greatest increases in Rs and Q10 were observed in arid areas, and the stimulation rates decreased with increases in climate humidity. When the decreased precipitation treatments were normalized to 28% below the ambient level, the soil moisture and Rs values decreased by an average of -14% and -17%, respectively, and the soil temperature and Q10 values were not altered. The reductions in soil moisture tended to be greater in more humid areas. Prolonged drought without alterations in the amount of precipitation reduced the soil moisture and Rs by -12% and -6%, respectively, but did not alter Q10. Overall, our synthesis suggests that soil moisture and Rs tend to be more sensitive to increased precipitation in more arid areas and more responsive to decreased precipitation in more humid areas. The responses of Rs and Q10 were predominantly driven by precipitation-induced changes in the soil moisture, whereas changes in the soil temperature had limited impacts. Finally, our synthesis of prolonged drought experiments also emphasizes the importance of the timing and frequency of precipitation events on ecosystem C cycles. Given these findings, we urge future studies to focus on manipulating the frequency, intensity, and seasonality of precipitation with an aim to improving our ability to predict and model feedback between Rs and climate change.

Darwinian sex roles confirmed across the animal kingdom

Consistent with Darwin’s ideas, this meta-analysis reveals that males experience stronger sexual selection than females. Since Darwin’s conception of sexual selection theory, scientists have struggled to identify the evolutionary forces underlying the pervasive differences between male and female behavior, morphology, and physiology. The Darwin-Bateman paradigm predicts that anisogamy imposes stronger sexual selection on males, which, in turn, drives the evolution of conventional sex roles in terms of female-biased parental care and male-biased sexual dimorphism. Although this paradigm forms the cornerstone of modern sexual selection theory, it still remains untested across the animal tree of life. This lack of evidence has promoted the rise of alternative hypotheses arguing that sex differences are entirely driven by environmental factors or chance. We demonstrate that, across the animal kingdom, sexual selection, as captured by standard Bateman metrics, is indeed stronger in males than in females and that it is evolutionarily tied to sex biases in parental care and sexual dimorphism. Our findings provide the first comprehensive evidence that Darwin’s concept of conventional sex roles is accurate and refute recent criticism of sexual selection theory.

Bias and correction for the log response ratio in ecological meta-analysis.

Ecologists widely use the log response ratio for summarizing the outcomes of studies for meta-analysis. However, little is known about the sampling distribution of this effect size estimator. Here I show with a Monte Carlo simulation that the log response ratio is biased when quantifying the outcome of studies with small sample sizes, and can yield erroneous variance estimates when the scale of study parameters are near zero. Given these challenges, I derive and compare two new estimators that help correct this small-sample bias, and update guidelines and diagnostics for assessing when the response ratio is appropriate for ecological meta-analysis. These new bias-corrected estimators retain much of the original utility of the response ratio and are aimed to improve the quality and reliability of inferences with effect sizes based on the log ratio of two means.