R-3 Repository :: Browsing by Author "Miller, Tom E.X."

Browsing by Author "Miller, Tom E.X."

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A comparative approach to testing hypotheses for the evolution of sex-biased dispersal in bean beetles
(Wiley, 2015) Downey, Michelle H.; Searle, Rebecca; Bellur, Sunil; Geiger, Adam; Maitner, Brian S.; Ohm, Johanna R.; Tuda, Midori; Miller, Tom E.X.
Understanding the selective forces that shape dispersal strategies is a fundamental goal of evolutionary ecology and is increasingly important in changing, human-altered environments. Sex-biased dispersal (SBD) is common in dioecious taxa, and understanding variation in the direction and magnitude of SBD across taxa has been a persistent challenge. We took a comparative, laboratory-based approach using 16 groups (species or strains) of bean beetles (generaﾠAcanthoscelides,ﾠCallosobruchus, andﾠZabrotes, including 10 strains of one species) to test two predictions that emerge from dominant hypotheses for the evolution of SBD: (1) groups that suffer greater costs of inbreeding should exhibit greater SBD in favor of either sex (inbreeding avoidance hypothesis) and (2) groups with stronger local mate competition should exhibit greater male bias in dispersal (kin competition avoidance hypothesis). We used laboratory experiments to quantify SBD in crawling dispersal, the fitness effects of inbreeding, and the degree of polygyny (number of female mates per male), a proxy for local mate competition. While we found that both polygyny and male-biased dispersal were common across bean beetle groups, consistent with the kin competition avoidance hypothesis, quantitative relationships between trait values did not support the predictions. Across groups, there was no significant association between SBD and effects of inbreeding nor SBD and degree of polygyny, using either raw values or phylogenetically independent contrasts. We discuss possible limitations of our experimental approach for detecting the predicted relationships, as well as reasons why single-factor hypotheses may be too simplistic to explain the evolution of SBD.
Avoiding unintentional eviction from integral projection models
(Ecological Society of America, 2012-09) Williams, Jennifer L.; Miller, Tom E.X.; Ellner, Stephen P.
Integral projection models (IPMs) are increasingly being applied to study size-structured populations. Here we call attention to a potential problem in their construction that can have important consequences for model results. IPMs are implemented using an approximating matrix and bounded size range. Individuals near the size limits can be unknowingly "evicted" from the model because their predicted future size is outside the range. We provide simple measures for the magnitude of eviction and the sensitivity of the population growth rate (lambda) to eviction, allowing modelers to assess the severity of the problem in their IPM. For IPMs of three plant species, we found that eviction occurred in all cases and caused underestimation of the population growth rate (lambda) relative to eviction-free models; it is likely that other models are similarly affected. Models with frequent eviction should be modified because eviction is only possible when size transitions are badly mis-specified. We offer several solutions to eviction problems, but we emphasize that the modeler must choose the most appropriate solution based on an understanding of why eviction occurs in the first place. We recommend testing IPMs for eviction problems and resolving them, so that population dynamics are modeled more accurately.
Balancing anti-herbivore benefits and anti-pollinator costs of defensive mutualists
(Ecological Society of America, 2014) Ohm, Johanna R.; Miller, Tom E.X.
Quantifying costs and benefits of ostensibly mutualistic interactions is an important step toward understanding their evolutionary trajectories. In food-for-protection interactions between ants and extrafloral nectar (EFN)-bearing plants, tending by aggressive ants may deter herbivores, but it may also deter pollinators. The fitness costs of pollinator deterrence are not straightforward for long-lived iteroparous plants, because reproductive vital rates often contribute weakly to fitness relative to growth and survival (vital rates that may be enhanced by ant defense). We used field manipulations of ant and pollinator activity and demographic modeling to examine how pollination costs of ant defense translate to plant fitness, given the benefits of ant defense elsewhere in the plant life cycle. We contrasted the net fitness effects of alternative ant partner species. Our work focused on the tree cholla cactus, Opuntia imbricata, an EFN-bearing plant associated with two ant species (Crematogaster opuntiae and Liometopum apiculatum) that differ in quality of defense against insect herbivores. We found that ant defense imposed pollination costs, despite evidence for ant-repellent floral volatiles and temporal partitioning of ant and pollinator activity. The two partner species similarly reduced pollinator visitation and seed mass, and one (C. opuntiae) additionally reduced seed number. We used the experimental data and other long-term demographic data to parameterize an integral projection model that integrated costs and benefits of ant defense over the complete plant life cycle. Model results indicated that the pollination costs of L. apiculatum were balanced by beneficial effects on growth, leading to a net fitness effect that was neutral to positive. By contrast, pollination costs outweighed benefits for C. opuntiae, the weaker defender, rendering this species a reproductive parasite. Thus, we infer that pollination costs destabilize mutualism with one partner species, but are offset by strong defensive benefits provided by the other, leading to contrasting selective pressures imposed by alternative associations. Accounting for ontogenetic turnover in ant partner identity indicated that most plants avoid the parasitic effects of C. opuntiae by associating nonrandomly with L. apiculatum at reproductive life stages. Our results highlight the value of a demographic approach to quantifying the costs and benefits of mutualism.
Consequences of sex-selective harvesting and harvest refuges in experimental meta-populations
(Nordic Society Oikos, 2013) Snyder, Kate T.; Freidenfelds, Nicole A.; Miller, Tom E.X.
Harvesting for food or sport is often non-random with respect to demographic state, such as size or life stage. The population- level consequences of such selective harvesting depend upon which states are harvested and how those states contribute to population dynamics. We focused on a form of selective harvesting that has not previously been investigated in an experimental context: sex-selective harvesting, a common feature of exploited, dioecious populations. Using simple metapopulations (two patches connect by dispersal) of sexually dimorphic Bruchid beetles in the laboratory, we contrasted the effects of female-selective, male-selective, and non-selective harvesting over six generation of population dynamics. We also tested the ability of a harvest refuge (one patch of the metapopulation free from harvesting) to mitigate the effects of harvesting, and whether refuge effects interacted with sex selectivity. Sex-selective harvesting significantly perturbed operational sex ratios and harvest refuges dampened these perturbations. Metapopulations assigned to male-selective and non-selective treatments were able to fully compensate for harvesting, such that their dynamics did not differ from non-harvested controls. Only female-selective harvesting led to significant reductions in population size and this effect was completely offset by dispersal from a harvest refuge. A two-sex model confirmed that population dynamics are more sensitive to female vs. male harvesting, but suggested that higher levels of male harvest than included in our experiment would cause population decline. We discuss the roles of density-dependent competition and frequency-dependent sexual processes in the population response to sex-selective harvesting.
Demographic causes of adult sex ratio variation and their consequences for parental cooperation
(Springer Nature, 2018) Eberhart-Phillips, Luke J.; Küpper, Clemens; Carmona-Isunza, María Cristina; Vincze, Orsolya; Zefania, Sama; Cruz-López, Medardo; Kosztolányi, András; Miller, Tom E.X.; Barta, Zoltán; Cuthill, Innes C.; Burke, Terry; Székely, Tamás; Hoffman, Joseph I.; Krüger, Oliver
The adult sex ratio (ASR) is a fundamental concept in population biology, sexual selection, and social evolution. However, it remains unclear which demographic processes generate ASR variation and how biases in ASR in turn affect social behaviour. Here, we evaluate the demographic mechanisms shaping ASR and their potential consequences for parental cooperation using detailed survival, fecundity, and behavioural data on 6119 individuals from six wild shorebird populations exhibiting flexible parental strategies. We show that these closely related populations express strikingly different ASRs, despite having similar ecologies and life histories, and that ASR variation is largely driven by sex differences in the apparent survival of juveniles. Furthermore, families in populations with biased ASRs were predominantly tended by a single parent, suggesting that parental cooperation breaks down with unbalanced sex ratios. Taken together, our results indicate that sex biases emerging during early life have profound consequences for social behaviour.
Does ant–plant mutualism have spillover effects on the non-partner ant community?
(Wiley, 2022) Donald, Marion L.; Miller, Tom E.X.; Program in Ecology and Evolutionary Biology
Mutualism benefits partner species, and theory predicts these partnerships can affect the abundance, diversity, and composition of partner and non-partner species. We used 16 years of monitoring data to determine the ant partner species of tree cholla cacti (Cylindropuntia imbricata), which reward ants with extrafloral nectar in exchange for anti-herbivore defense. These long-term data revealed one dominant ant partner (Liometopum apiculatum) and two less common partners (Crematogaster opuntiae and Forelius pruinosus). We then used short-term characterization of the terrestrial ant community by pitfall trapping to sample partner and non-partner ant species across ten plots of varying cactus density. We found that the dominant ant partner tended a higher proportion cacti in plots of higher cactus density, and was also found at higher occurrence within the pitfall traps in higher density plots, suggesting a strong positive feedback that promotes ant partner occurrence where plant partners are available. Despite the strong association and increased partner occurrence, ant community-wide effects from this mutualism appear limited. Of the common ant species, the occurrence of a single non-partner ant species was negatively associated with cactus density and with the increased presence of L. apiculatum. Additionally, the composition and diversity of the ant community in our plots were insensitive to cactus density variation, indicating that positive effects of the mutualism on the dominant ant partner did not have cascading impacts on the ant community. This study provides novel evidence that exclusive mutualisms, even those with a strong positive feedback, may be limited in the scope of their community-level effects.
Lagged and dormant season climate better predict plant vital rates than climate during the growing season
(Wiley, 2021) Evers, Sanne M.; Knight, Tiffany M.; Inouye, David W.; Miller, Tom E.X.; Salguero‐Gómez, Roberto; Iler, Amy M.; Compagnoni, Aldo; Program in Ecology and Evolutionary Biology
Understanding the effects of climate on the vital rates (e.g., survival, development, reproduction) and dynamics of natural populations is a long-standing quest in ecology, with ever-increasing relevance in the face of climate change. However, linking climate drivers to demographic processes requires identifying the appropriate time windows during which climate influences vital rates. Researchers often do not have access to the long-term data required to test a large number of windows, and are thus forced to make a priori choices. In this study, we first synthesize the literature to assess current a priori choices employed in studies performed on 104 plant species that link climate drivers with demographic responses. Second, we use a sliding-window approach to investigate which combination of climate drivers and temporal window have the best predictive ability for vital rates of four perennial plant species that each have over a decade of demographic data (Helianthella quinquenervis, Frasera speciosa, Cylindriopuntia imbricata, and Cryptantha flava). Our literature review shows that most studies consider time windows in only the year preceding the measurement of the vital rate(s) of interest, and focus on annual or growing season temporal scales. In contrast, our sliding-window analysis shows that in only four out of 13 vital rates the selected climate drivers have time windows that align with, or are similar to, the growing season. For many vital rates, the best window lagged more than 1 year and up to 4 years before the measurement of the vital rate. Our results demonstrate that for the vital rates of these four species, climate drivers that are lagged or outside of the growing season are the norm. Our study suggests that considering climatic predictors that fall outside of the most recent growing season will improve our understanding of how climate affects population dynamics.
Mammalian herbivores restrict the altitudinal range limits of alpine plants
(Wiley, 2021) Lynn, Joshua S.; Miller, Tom E.X.; Rudgers, Jennifer A.
Although rarely experimentally tested, biotic interactions have long been hypothesised to limit low-elevation range boundaries of species. We tested the effects of herbivory on three alpine-restricted plant species by transplanting plants below (novel), at the edge (limit), or in the centre (core) of their current elevational range and factorially fencing-out above- and belowground mammals. Herbivore damage was greater in range limit and novel habitats than in range cores. Exclosures increased plant biomass and reproduction more in novel habitats than in range cores, suggesting demographic costs of novel interactions with herbivores. We then used demographic models to project population growth rates, which increased 5–20% more under herbivore exclosure at range limit and novel sites than in core habitats. Our results identify mammalian herbivores as key drivers of the low-elevation range limits of alpine plants and indicate that upward encroachment of herbivores could trigger local extinctions by depressing plant population growth.
Nectar resources affect bird-dispersed microbial metacommunities in suburban and rural gardens
(Wiley, 2022) Donald, Marion L.; Galbraith, Josie A.; Erastova, Daria A.; Podolyan, Anastasija; Miller, Tom E.X.; Dhami, Manpreet K.
As cities expand, understanding how urbanization affects biodiversity is a key ecological goal. Yet, little is known about how host-associated microbial diversity responds to urbanization. We asked whether communities of microbial (bacterial and fungal) in floral nectar and sugar-water feeders and vectored by nectar-feeding birds—thus forming a metacommunity—differed in composition and diversity between suburban and rural gardens. Compared to rural birds, we found that suburban birds vectored different and more diverse bacterial communities. These differences were not detected in the nectar of common plant species, suggesting that nectar filters microbial taxa and results in metacommunity convergence. However, when considering all the nectar sources present, suburban beta diversity was elevated compared to rural beta diversity due to turnover of bacterial taxa across a plant species and sugar-water feeders. While fungal metacommunity composition and beta diversity in nectar were similar between suburban and rural sites, alpha diversity was elevated in suburban sites, which mirrored the trend of increased fungal alpha diversity on birds. These results emphasize the interdependence of host, vector, and microbial diversity and demonstrate that human decisions can shape nectar microbial diversity in contrasting ways for bacteria and fungi.
Niche Differentiation in the Dynamics of Host-Symbiont Interactions: Symbiont Prevalence as a Coexistence Problem
(The University of Chicago Press, 2014-04) Miller, Tom E.X.; Rudgers, Jennifer A.
Heritable symbioses can have important ecological effects and have triggered important evolutionary innovations. Current predictions for long-term symbiont prevalence are based on their fitness benefits and vertical transmission rates but ignore nonlinear competitive feedbacks among symbiotic and symbiont-free hosts. We hypothesized that such feedbacks function as stabilizing mechanisms, promoting coexistence of host types and maintaining intermediate symbiont frequency at the population scale. Using a model grass/endophyte symbiosis, we manipulated competition within and between endophyte-symbiotic (E+) and endophyte-free (E-) hosts and fit competition models to experimental data. We show for the first time that symbiont-structured competition can generate stable coexistence of E+ and E- hosts, even under perfect vertical transmission. Niche differentiation was the key to coexistence, causing hosts of each type to limit themselves more strongly than each other. These results establish roles for nonlinear competitive dynamics and niche differentiation in the ecology and evolution of heritable symbionts.
Plant size and reproductive state affect the quantity and quality of rewards to animal mutualists
(British Ecological Society, 2014) Miller, Tom E.X.
Many plants engage ants in defensive mutualisms by offering extrafloral nectar (EFN). Identifying sources of variation in EFN quantity (amount) and quality (composition) is important because they can affect ant visitation and identity and hence effectiveness of plant defence. I investigated plant size and reproductive state (vegetative or flowering) as sources of variation in EFN quantity and quality. I focused on Opuntia imbricata and two ant partners, Crematogaster opuntiae and Liometopum apiculatum. I tested the influence of plant size and nectary type (vegetative vs. reproductive structure) on the probability and rate of EFN secretion, concentrations of total carbohydrates (CH) and amino acids (AAs), and relative abundances of constituent CH and AAs. I also examined how traits of individual nectaries scaled up to influence total plant-level rewards. Parallel observations documented associations between plant demographic state and ant visitation and species identity. EFN quantity and quality were generally greater for larger, reproductive plants. At the scale of individual nectaries, probability of EFN secretion was positively size-dependent and greater for nectaries on reproductive vs. vegetative structures. Rate of EFN secretion, carbohydrate and amino acid concentrations, and the relative abundance of disaccharide vs. monosaccharide sugars were greater for reproductive nectaries but were unaffected by plant size. Nectary-level traits scaled up to influence rewards at the whole-plant level in ways that corresponded to ant visitation: the probability of ant occupancy increased with plant size and reproduction, as did the likelihood of being tended by the superior guard, L. apiculatum. Variability in EFN traits may contribute to changes in ant occupancy and identity across plant sizes and reproductive states. Synthesis. This study provides a thorough examination of how plant investment in biotic defence varies over the life cycle. Explicit consideration of plant demography may enhance understanding of ant?plant mutualisms. Populations of long-lived plants are demographically heterogeneous, spanning sizes and reproductive states. The rewards offered to animal mutualists can track demographic heterogeneity with consequences for plant defence and the dynamics of multispecies mutualisms.
Population Dynamics of Heritable Symbionts when Accounting for the Life History Complexity of their Host
(2015-06-12) Bibian, Andrew James; Miller, Tom E.X.; Dunham, Amy; Rudolph, Volker
I developed theory and experiments to understand how complex life cycles of a host affect the dynamics of their heritable symbionts, important ecological and evolutionary agents. With symbiont persistence and prevalence being a function of their effects on host fitness and transmission efficiencies, accounting for host demographic “storage,” in the form of non-reproductive or dormant host life stages, leads to unexpected results. Symbiont loss from demographic storage affects persistence similarly to loss from a host reproductive stage. Loss from host dormancy, however, affect dynamics if symbiont passage through the dormant stage occurs at a high rate, which we observed with experiments. Demographic rescue and symbiont persistence was possible, and observed, whereby stage specific symbiont benefits compensate for symbiont loss. Empirically, accounting for host dormancy in the form of a plant seed bank facilitated symbiont persistence and prevalence. Our results emphasize the importance of accounting for realistic complexity in host-symbiont dynamics.
Rapid evolution of dispersal ability makes biological invasions faster and more variable
(Springer Nature, 2017) Ochocki, Brad M.; Miller, Tom E.X.
Genetic variation in dispersal ability may result in the spatial sorting of alleles during range expansion. Recent theory suggests that spatial sorting can favour the rapid evolution of life history traits at expanding fronts, and therefore modify the ecological dynamics of range expansion. Here we test this prediction by disrupting spatial sorting in replicated invasions of the bean beetleﾠCallosobruchus maculatusﾠacross homogeneous experimental landscapes. We show that spatial sorting promotes rapid evolution of dispersal distance, which increases the speed and variability of replicated invasions: after 10 generations of range expansion, invasions subject to spatial sorting spread 8.9% farther and exhibit 41-fold more variable spread dynamics relative to invasions in which spatial sorting is suppressed. Correspondingly, descendants from spatially evolving invasions exhibit greater mean and variance in dispersal distance. Our results reveal an important role for rapid evolution during invasion, even in the absence of environmental filters, and argue for evolutionarily informed forecasts of invasive spread by exotic species or climate change migration by native species.
Sex and stochasticity affect range expansion of experimental invasions
(Blackwell Publishing, 2012) Miller, Tom E.X.; Inouye, Brian D.
The effect of demographic correlations on the stochastic population dynamics of perennial plants
(Ecological Society of America, 2016) Compagnoni, Aldo; Bibian, Andrew J.; Ochocki, Brad M.; Rogers, Haldre S.; Schultz, Emily L.; Sneck, Michelle E.; Elderd, Bret D.; Iler, Amy M.; Inouye, David W.; Jacquemyn, Hans; Miller, Tom E.X.
Understanding the influence of environmental variability on population dynamics is a fundamental goal of ecology. Theory suggests that, for populations in variable environments, temporal correlations between demographic vital rates (e.g., growth, survival, reproduction) can increase (if positive) or decrease (if negative) the variability of year-to-year population growth. Because this variability generally decreases long-term population viability, vital rate correlations may importantly affect population dynamics in stochastic environments. Despite long-standing theoretical interest, it is unclear whether vital rate correlations are common in nature, whether their directions are predominantly negative or positive, and whether they are of sufficient magnitude to warrant broad consideration in studies of stochastic population dynamics. We used long-term demographic data for three perennial plant species, hierarchical Bayesian parameterization of population projection models, and stochastic simulations to address the following questions: (1) What are the sign, magnitude, and uncertainty of temporal correlations between vital rates? (2) How do specific pairwise correlations affect the year-to-year variability of population growth? (3) Does the net effect of all vital rate correlations increase or decrease year-to-year variability? (4) What is the net effect of vital rate correlations on the long-term stochastic population growth rate (λs)? We found only four moderate to strong correlations, both positive and negative in sign, across all species and vital rate pairs; otherwise, correlations were generally weak in magnitude and variable in sign. The net effect of vital rate correlations ranged from a slight decrease to an increase in the year-to-year variability of population growth, with average changes in variance ranging from −1% to +22%. However, vital rate correlations caused virtually no change in the estimates of λs (mean effects ranging from −0.01% to +0.17%). Therefore, the proportional changes in the variance of population growth caused by demographic correlations were too small on an absolute scale to importantly affect population growth and viability. We conclude that, in our three focal populations and perhaps more generally, vital rate correlations have little effect on stochastic population dynamics. This may be good news for population ecologists, because estimating vital rate correlations and incorporating them into population models can be data intensive and technically challenging.
The Role of Host Demographic Storage in the Ecological Dynamics of Heritable Symbionts
(The University of Chicago Press, 2016) Bibian, Andrew J.; Rudgers, Jennifer A.; Miller, Tom E.X.
Heritable symbioses are widespread and ecologically important. Many host organisms have complex life cycles that include diverse opportunities for symbionts to affect their host and be lost during development. Yet, existing theory takes a simplified view of host demography. Here, we generalize symbiosis theory to understand how demographic “storage” in the form of dormant or prereproductive life stages can modify symbiosis dynamics. Using grass-endophyte symbioses as context, we developed models to contrast the role of the seed bank (a storage stage) against the reproductive stage in symbiont persistence and prevalence. We find that the seed bank is as important as or more important than the reproductive stage in driving symbiont dynamics, as long as passage through the seed bank is obligate. Flexible entry to the seed bank substantially weakens its influence on symbiont persistence but can modify prevalence in counterintuitive ways. Our models identify a role for legacy effects, where hosts that lose symbionts retain their demographic influence. The retention of benefits via legacy effects can reduce symbiont prevalence and even cause prevalence to decline with increasing benefits to hosts because symbiont-free hosts carry those benefits. Our results resolve connections between individual-level host-symbiont interactions and population-level patterns, providing guidance for empirical studies.

Browsing by Author "Miller, Tom E.X."

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