The evolution of imperfect mimicry in hoverflies

Ideas about the evolution of imperfect mimicry are reviewed. Their relevance to the colours patterns of hoverflies (Diptera, Syrphidae) are discussed in detail. Most if not all of the hoverflies labelled as mimetic actually are mimics. The apparently poor nature of their resemblance does not prevent them from obtaining at least some protection from suitably experienced birds. Mimicry is a dominant theme of this very large family of Diptera, with at least a quarter of all species in Europe being mimetic. Hoverfly mimics fall into three major groups according to their models, involving bumblebees, honeybees and social wasps. There are striking differences in the general levels of mimetic fidelity and relative abundances of the three groups, with accurate mimicry, low abundance and polymorphism characterizing the bumblebee mimics: more than half of all the species of bumblebee mimics are polymorphic. Mimics of social wasps tend to be poor mimics, have high relative abundance, and polymorphism is completely absent. Bumblebee models fall into a small number of Muellerian mimicry rings which are very different between the Palaearctic and Nearctic regions. Social wasps and associated models form one large Muellerian complex. Together with honeybees, these complexes probably form real clusters of forms as perceived by many birds. All three groups of syrphid mimics contain both good and poor mimics; some mimics are remarkably accurate, and have close morphological and behavioural resemblance. At least some apparently 'poor' mimetic resemblances may be much closer in birds' perception than we imagine, and more work needs to be done on this. Bumblebees are the least noxious and wasps the most noxious of the three main model groups. The basis of noxiousness is different, with bumblebees being classified as non-food, whereas honeybees and wasps are nasty-tasting and (rarely) stinging. The distribution of mimicry is exactly what would be expected from this ordering, with polymorphic and accurate forms being a key feature of mimics of the least noxious models, while highly noxious models have poor-quality mimicry. Even if the high abundance of many syrphid mimics relative to their models is a recent artefact of man-made environmental change, this does not preclude these species from being mimics. It seems unlikely that bird predation actually controls the populations of adult syrphids. Being rare relative to a model may have promoted or accelerated the evolution of perfect mimicry: theoretically this might account for the pattern of rare good mimics and abundant poor ones, but the idea is intrinsically unlikely. Many mimics seem to have hour-to-hour abundances related to those of their models, presumably as a result of behavioural convergence. We need to know much more about the psychology of birds as predators. There are at least four processes that need elucidating: (a) learning about the noxiousness of models; (b) the erasing of that learning through contact with mimics (extinction, or learned forgetting); (c) forgetting; (d) deliberate risk-taking and the physiological states that promote it. Johnston's (2002) model of the stabilization of imperfect mimicry by kin selection is unlikely to account for the colour patterns of hoverflies. Sherratt's (2002) model of the influence of multiple models potentially accounts for all the patterns of hoverfly mimicry, and is the most promising avenue for testing.

Annotation of Gyrodactylus salaris transcriptome

Relationship between organisms within an ecosystem is one of the main focuses in the study of ecology and evolution. For instance, host-parasite interactions have long been under close interest of ecology, evolutionary biology and conservation science, due to great variety of strategies and interaction outcomes. The monogenean ecto-parasites consist of a significant portion of flatworms. Gyrodactylus salaris is a monogenean freshwater ecto-parasite of Atlantic salmon (Salmo salar) whose damage can make fish to be prone to further bacterial and fungal infections. G. salaris is the only one parasite whose genome has been studied so far. The RNA-seq data analyzed in this thesis has already been annotated by using LAST. The RNA-seq data was obtained from Illumina sequencing i.e. yielded reads were assembled into 15777 transcripts. Last resulted in annotation of 46% transcripts and remaining were left unknown. This thesis work was started with whole data and annotation process was continued by the use of PANNZER, CDD and InterProScan. This annotation resulted in 56% successfully annotated sequences having parasite specific proteins identified. This thesis represents the first of Monogenean transcriptomic information which gives an important source for further research on this specie. Additionally, comparison of annotation methods interestingly revealed that description and domain based methods perform better than simple similarity search methods. Therefore it is more likely to suggest the use of these tools and databases for functional annotation. These results also emphasize the need for use of multiple methods and databases. It also highlights the need of more genomic information related to G. salaris.

Reorganisation ofHoxdregulatory landscapes during the evolution of a snake-like body plan

Within land vertebrate species, snakes display extreme variations in their body plan, characterized by the absence of limbs and an elongated morphology. Such a particular interpretation of the basic vertebrate body architecture has often been associated with changes in the function or regulation of Hox genes. Here, we use an interspecies comparative approach to investigate different regulatory aspects at the snake HoxD locus. We report that, unlike in other vertebrates, snake mesoderm-specific enhancers are mostly located within the HoxD cluster itself rather than outside. In addition, despite both the absence of limbs and an altered Hoxd gene regulation in external genitalia, the limb-associated bimodal HoxD chromatin structure is maintained at the snake locus. Finally, we show that snake and mouse orthologous enhancer sequences can display distinct expression specificities. These results show that vertebrate morphological evolution likely involved extensive reorganisation at Hox loci, yet within a generally conserved regulatory framework.

Contrasting effects of historical contingency on phenotypic and genomic trajectories during a two-step evolution experiment with bacteria

Background The impact of historical contingency, i.e. the past evolutionary history of a population, on further adaptation is mostly unknown at both the phenotypic and genomic levels. We addressed this question using a two-step evolution experiment. First, replicate populations of Escherichia coli were propagated in four different environmental conditions for 1000 generations. Then, all replicate populations were transferred and propagated for further 1000 generations to a single new environment. Results Using this two-step experimental evolution strategy, we investigated, at both the phenotypic and genomic levels, whether and how adaptation in the initial historical environments impacted evolutionary trajectories in a new environment. We showed that both the growth rate and fitness of the evolved populations obtained after the second step of evolution were contingent upon past evolutionary history. In contrast however, the genes that were modified during the second step of evolution were independent from the previous history of the populations. Conclusions Our work suggests that historical contingency affects phenotypic adaptation to a new environment. This was however not reflected at the genomic level implying complex relationships between environmental factors and the genotype-to-phenotype map.

Using a Combination of Phylogenetic Comparative and Paleobotanical Methods to Elucidate Patterns of Lineage Selection in Rosales (Plantae: Anthophyta)

An increasing focus in evolutionary biology is on the interplay between mesoscale ecological and evolutionary processes such as population demographics, habitat tolerance, and especially geographic distribution, as potential drivers responsible for patterns of diversification and extinction over geologic time. However, few studies to date connect organismal processes such as survival and reproduction through mesoscale patterns to long-term macroevolutionary trends. In my dissertation, I investigate how mechanism of seed dispersal, mediated through geographic range size, influences diversification rates in the Rosales (Plantae: Anthophyta). In my first chapter, I validate the phylogenetic comparative methods that I use in my second and third chapters. Available state speciation and extinction (SSE) models assumptions about evolution known to be false through fossil data. I show, however, that as long as net diversification rates remain positive – a condition likely true for the Rosales – these violations of SSE’s assumptions do not cause significantly biased results. With SSE methods validated, my second chapter reconstructs three associations that appear to increase diversification rate for Rosalean genera: (1) herbaceous habit; (2) a three-way interaction combining animal dispersal, high within-genus species richness, and geographic range on multiple continents; (3) a four-way interaction combining woody habit with the other three characteristics of (2). I suggest that the three- and four-way interactions represent colonization ability and resulting extinction resistance in the face of late Cenozoic climate change; however, there are other possibilities as well that I hope to investigate in future research. My third chapter reconstructs the phylogeographic history of the Rosales using both non-fossil-assisted SSE methods as well as fossil-informed traditional phylogeographic analysis. Ancestral state reconstructions indicate that the Rosaceae diversified in North America while the other Rosalean families diversified elsewhere, possibly in Eurasia. SSE is able to successfully identify groups of genera that were likely to have been ancestrally widespread, but has poorer taxonomic resolution than methods that use fossil data. In conclusion, these chapters together suggest several potential causal links between organismal, mesoscale, and geologic scale processes, but further work will be needed to test the hypotheses that I raise here.

Plant-mediated effects on microbial diversity in mesocosms of an oligotrophic bog

Globally, peatlands occupy a small portion of terrestrial land area but contain up to one-third of all soil organic carbon. This carbon pool is vulnerable to increased decomposition under projected climate change scenarios but little is known about how plant functional groups will influence microbial communities responsible for regulating carbon cycling processes. Here we examined initial shifts in microbial community structure within two sampling depths under plant functional group manipulations in mesocosms of an oligotrophic bog. Microbial community composition for bacteria and archaea was characterized using targeted 16S rRNA Illumina gene sequencing. We found statistically distinct spatial patterns between the more shallow 10-20 cm sampling depth and the deeper 30-40 cm depth. Significant effects by plant functional groups were found only within the 10-20 cm depth, indicating plant-mediated microbial community shifts respond more quickly near the peat surface. Specifically, the relative abundance of Acidobacteria decreased under ericaceous shrub treatments in the 10-20 cm depth and was replaced by increased abundance of Gammaproteobacteria and Bacteroidetes. In contrast, the sedge rhizosphere continued to be dominated by Acidobacteria but also promoted an increase in the relative recovery of Alphaproteobacteria and Verrucomicrobia. These initial results suggest microbial communities under ericaceous shrubs may be limited by anaerobic soil conditions accompanying high water table conditions, while sedge aerenchyma may be promoting aerobic taxa in the upper peat rhizosphere regardless of ambient soil oxygen limitations.

USING INDICATORS OF BIOTIC INTEGRITY FOR ASSESSMENT OF STREAM CONDITION

Multiple indices of biotic integrity and biological condition gradient models have been developed and validated to assess ecological integrity in the Laurentian Great Lakes Region. With multiple groups such as Tribal, Federal, and State agencies as well as scientists and local watershed management or river-focused volunteer groups collecting data for bioassessment it is important that we determine the comparability of data and the effectiveness of indices applied to these data for assessment of natural systems. We evaluated the applicability of macroinvertebrate and fish community indices for assessing site integrity. Site quality (i.e., habitat condition) could be classified differently depending on which index was applied. This highlights the need to better understand the metrics driving index variation as well as reference conditions for effective communication and use of indices of biotic integrity in the Upper Midwest. We found the macroinvertebrate benthic community index for the Northern Lakes and Forests Ecoregion and a coldwater fish index of biotic integrity for the Upper Midwest were most appropriate for use in the Big Manistee River watershed based on replicate sampling, ability to track trends over time and overall performance. We evaluated three sites where improper road stream crossings (culverts) were improved by replacing them with modern full-span structures using the most appropriate fish and macroinvertebrate IBIs. We used a before-after-control-impact paired series analytical design and found mixed results, with evidence of improvement in biotic integrity based on macroinvertebrate indices at some of the sites while most sites indicated no response in index score. Culvert replacements are often developed based on the potential, or the perception, that they will restore ecological integrity. As restoration practitioners, researchers and managers, we need to be transparent in our goals and objectives and monitor for those results specifically. The results of this research serve as an important model for the broader field of ecosystem restoration and support the argument that while biotic communities can respond to actions undertaken with the goal of overall restoration, practitioners should be realistic in their expectations and claims of predicted benefit, and then effectively evaluate the true impacts of the restoration activities.

EVALUATION AND MONITORING OF ASH (FRAXINUS SPP.) TOLERANT TO LONG-TERM EMERALD ASH BORER (AGRILUS PLANIPENNIS [COLEOPTERA: BUPRESTIDAE]) EXPOSURE

Invasive insects that successfully establish in introduced areas can significantly alter natural communities. These pests require specific establishment criteria (e.g. host suitability) that, when known, can help quantify potential damage to infested areas. Emerald ash borer (Agrilus planipennis [Coleoptera: Buprestidae]) is an invasive phloem-feeding pest which is responsible for the death of millions of ash trees (Fraxinus spp. L.). Over 200 surviving ash trees were previously identified in the Huron-Clinton Metroparks located in southeast Michigan. Trees were assessed over a four year period and a hierarchical cluster analysis was performed on dieback, vigor, and presence of signs and symptoms, in order to place trees into one of three tolerance groups. The clustering of trees with different responses to emerald ash borer attack suggests that there are different tolerance levels in North American ash trees in southeastern Michigan, and these groups were designated as apparently tolerant, not tolerant and intermediate tolerance. Adult landing rates and evidence of adult emergence were significantly lower in the apparently tolerant group compared with the not tolerant group, but larval survival from eggs placed on trees did not differ between tolerance groups. Therefore, it appears that apparently tolerant trees survive because they are less attractive to adult beetles which results in fewer eggs being laid on them. Trees in the apparently tolerant group remained of higher vigor over the four years of the study. North American ash may survive the emerald ash borer epidemic due to natural variation and inherent resistance regardless of the lack of co-evolutionary history with emerald ash borer.

ANALYSIS OF POPULUS TREMULOIDES CLONAL VARIATION AND DELINEATION IN THE OTTAWA NATIONAL FOREST

The technique of delineating Populus tremuloides (Michx.) clonal colonies based on morphology and phenology has been utilized in many studies and forestry applications since the 1950s. Recently, the availability and robustness of molecular markers has challenged the validity of such approaches for accurate clonal identification. However, genetically sampling an entire stand is largely impractical or impossible. For that reason, it is often necessary to delineate putative genet boundaries for a more selective approach when genetically analyzing a clonal population. Here I re-evaluated the usefulness of phenotypic delineation by: (1) genetically identifying clonal colonies using nuclear microsatellite markers, (2) assessing phenotypic inter- and intraclonal agreement, and (3) determining the accuracy of visible characters to correctly assign ramets to their respective genets. The long-term soil productivity study plot 28 was chosen for analysis and is located in the Ottawa National Forest, MI (46° 37'60.0" N, 89° 12'42.7" W). In total, 32 genets were identified from 181 stems using seven microsatellite markers. The average genet size was 5.5 ramets and six of the largest were selected for phenotypic analyses. Phenotypic analyses included budbreak timing, DBH, bark thickness, bark color or brightness, leaf senescence, leaf serrations, and leaf length ratio. All phenotypic characters, except for DBH, were useful for the analysis of inter- and intraclonal variation and phenotypic delineation. Generally, phenotypic expression was related to genotype with multiple response permutation procedure (MRPP) intraclonal distance values ranging from 0.148 and 0.427 and an observed MRPP delta value=0.221 when the expected delta=0.5. The phenotypic traits, though, overlapped significantly among some clones. When stems were assigned into phenotypic groups, six phenotypic groups were identified with each group containing a dominant genotype or clonal colony. All phenotypic groups contained stems from at least two clonal colonies and no clonal colony was entirely contained within one phenotypic group. These results demonstrate that phenotype varies with genotype and stand clonality can be determined using phenotypic characters, but phenotypic delineation is less precise. I therefore recommend that some genetic identification follow any phenotypic delineation. The amount of genetic identification required for clonal confirmation is likely to vary based on stand and environmental conditions. Further analysis, however, is needed to test these findings in other forest stands and populations.

IONIC LIQUID EXTRACTION UNVEILS PREVIOUSLY OCCLUDED HUMICBOUND IRON IN PEAT POREWATER

Extracellular iron reduction has been suggested as a candidate metabolic pathway that may explain a large proportion of carbon respiration in temperate peatlands. However, the o-phenanthroline colorimetric method commonly employed to quantitate iron and partition between redox species is known to be unreliable in the presence of humic and fulvic acids, both of which represent a considerable proportion of peatland dissolved organic matter. We propose ionic liquid extraction as a more accurate iron quantitation and redox speciation method in humic-rich peat porewater. We evaluated both o-phenanthroline and ionic liquid extraction in four distinct peatland systems spanning a gradient of physico-chemical conditions to compare total iron recovery and Fe2+:Fe3+ ratios determined by each method. Ionic liquid extraction was found to provide more accurate iron quantitation and speciation in the presence of dissolved organic matter. A multivariate approach utilizing fluorescence- and UV-Vis spectroscopy was used to identify dissolved organic matter characteristics in peat porewater that lead to poor performance of the o-phenanthroline method. Where these interferences are present, we offer an empirical correction factor for total iron quantitation by o-phenanthroline, as verified by ionic liquid extraction. The written work presented in this thesis is in preparation for submission to Soil Biology and Biochemisrty by T.J. Veverica, E.S. Kane, A.M. Marcarelli, and S.A. Green.

Big Manistee River Tributaries as Potential Arctic Grayling Habitat

The Big Manistee River was one of the most well known Michigan rivers to historically support a population of Arctic grayling (Thymallus arctics). Overfishing, competition with introduced fish, and habitat loss due to logging are believed to have caused their decline and ultimate extirpation from the Big Manistee River around 1900 and from the State of Michigan by 1936. Grayling are a species of great cultural importance to Little River Band of Ottawa Indian tribal heritage and although past attempts to reintroduce Arctic grayling have been unsuccessful, a continued interest in their return led to the assessment of environmental conditions of tributaries within a 21 kilometer section of the Big Manistee River to determine if suitable habitat exists. Although data describing historical conditions in the Big Manistee River is limited, we reviewed the literature to determine abiotic conditions prior to Arctic grayling disappearance and the habitat conditions in rivers in western and northwestern North America where they currently exist. We assessed abiotic habitat metrics from 23 sites distributed across 8 tributaries within the Manistee River watershed. Data collected included basic water parameters, streambed substrate composition, channel profile and areal measurements of channel geomorphic unit, and stream velocity and discharge measurements. These environmental condition values were compared to literature values, habitat suitability thresholds, and current conditions of rivers with Arctic grayling populations to assess the feasibility of the abiotic habitat in Big Manistee River tributaries to support Arctic grayling. Although the historic grayling habitat in the region was disturbed during the era of major logging around the turn of the 20th century, our results indicate that some important abiotic conditions within Big Manistee River tributaries are within the range of conditions that support current and past populations of Arctic grayling. Seven tributaries contained between 20-30% pools by area, used by grayling for refuge. All but two tributaries were composed primarily of pebbles, with the remaining two dominated by fine substrates (sand, silt, clay). Basic water parameters and channel depth were within the ranges of those found for populations of Arctic grayling persisting in Montana, Alaska, and Canada for all tributaries. Based on the metrics analyzed in this study, suitable abiotic grayling habitat does exist in Big Manistee River tributaries.

Influence of Vegetation Removal and Altering Water Levels on CO2 Flux Rates of a Northern Bog

Boreal peatlands contain approximately one third of the global soil carbon and are considered net sinks of atmospheric CO2. Water level position is one of the main regulators of CO2 fluxes in northern peatlands because it controls both the thickness of the aerobic layer in peat and plant communities. However, little is known about the role of different plant functional groups and their possible interaction with changing water level in boreal peatlands with regard to CO2 cycling. Climate change may also accelerate changes in hydrological conditions, changing both aerobic conditions and plant communities. To help answer these questions, this study was conducted at a mesocosm facility in Northern Michigan where the aim was to experimentally study the effects of water levels, plant functional groups (sedges, shrubs and mosses) and the possible interaction of these on the CO2 cycle of a boreal peatland ecosystem. The results indicate that Ericaceous shrubs are important in the boreal peatland CO2 cycle. The removal of these plants decreased ecosystem respiration, gross ecosystem production and net ecosystem exchange rates, whereas removing sedges did not show any significant differences in the flux rates. The water level did not significantly affect the flux rates. The amount of aboveground sedge biomass was higher in the low water level sedge treatment plots compared to the high water level sedge plots, possibly because the lowered water level and the removal of Ericaceae released nutrients for sedges to use up.

INTERACTIVE EFFECTS OF CLIMATE CHANGE AND FUNGAL COMMUNITIES ON THE DECOMPOSITION OF WOOD-DERIVED CARBON IN FOREST SOILS

Soils are the largest sinks of carbon in terrestrial ecosystems. Soil organic carbon is important for ecosystem balance as it supplies plants with nutrients, maintains soil structure, and helps control the exchange of CO2 with the atmosphere. The processes in which wood carbon is stabilized and destabilized in forest soils is still not understood completely. This study attempts to measure early wood decomposition by different fungal communities (inoculation with pure colonies of brown or white rot, or the original microbial community) under various interacting treatments: wood quality (wood from +CO2, +CO2+O3, or ambient atmosphere Aspen-FACE treatments from Rhinelander, WI), temperature (ambient or warmed), soil texture (loamy or sandy textured soil), and wood location (plot surface or buried 15cm below surface). Control plots with no wood chips added were also monitored throughout the study. By using isotopically-labelled wood chips from the Aspen-FACE experiment, we are able to track wood-derived carbon losses as soil CO2 efflux and as leached dissolved organic carbon (DOC). We analyzed soil water for chemical characteristics such as, total phenolics, SUVA254, humification, and molecular size. Wood chip samples were also analyzed for their proportion of lignin:carbohydrates using FTIR analysis at three time intervals throughout 12 months of decomposition. After two years of measurements, the average total soil CO2 efflux rates were significantly different depending on wood location, temperature, and wood quality. The wood-derived portion soil CO2 efflux also varied significantly by wood location, temperature, and wood quality. The average total DOC and the wood-derived portion of DOC differed between inoculation treatments, wood location, and temperature. Soil water chemical characteristics varied significantly by inoculation treatments, temperature, and wood quality. After 12 months of decomposition the proportion of lignin:carbohydrates varied significantly by inoculation treatment, with white rot having the only average proportional decrease in lignin:carbohydrates. Both soil CO2 efflux and DOC losses indicate that wood location is important. Carbon losses were greater from surface wood chips compared with buried wood chips, implying the importance of buried wood for total ecosystem carbon stabilization. Treatments associated with climate change also had an effect on the level of decomposition. DOC losses, soil water characteristics, and FTIR data demonstrate the importance of fungal community on the degree of decomposition and the resulting byproducts found throughout the soil.

Root:Shoot Ratio and Specific Leaf Area Along an Elevational Gradient in the Peruvian Andes

Andean montane forests are one of the most diverse ecosystems on Earth, but are also highly vulnerable to climate change. Therefore, the link between plant distribution and ecosystem productivity is a critical point to investigate in these ecosystems. Are the patterns in productivity observed in montane forest due to species turnover along the elevational gradients? Methodological constraints keep this question unanswered. Also, despite their importance, belowground biomass remains poorly quantified and understood. I measured two plant functional traits in seedlings, root:shoot ratio and specific leaf area, to identify different strategies in growth and biomass allocation across elevations. A tradeoff in specific leaf area with elevation was found in only one species, and no generalized directional change was detected with elevations for root:shoot ratio. Lack of information for the ontogeny of the measured plant traits could confounding the analysis.

Factors Influencing Movements and Foraging Ecology of American Alligators (Alligator mississippiensis) in a Dynamic Subtropical Coastal Ecosystem

Top predators can have large effects on community and population dynamics but we still know relatively little about their roles in ecosystems and which biotic and abiotic factors potentially affect their behavioral patterns. Understanding the roles played by top predators is a pressing issue because many top predator populations around the world are declining rapidly yet we do not fully understand what the consequences of their potential extirpation could be for ecosystem structure and function. In addition, individual behavioral specialization is commonplace across many taxa, but studies of its prevalence, causes, and consequences in top predator populations are lacking. In this dissertation I investigated the movement, feeding patterns, and drivers and implications of individual specialization in an American alligator (Alligator mississippiensis) population inhabiting a dynamic subtropical estuary. I found that alligator movement and feeding behaviors in this population were largely regulated by a combination of biotic and abiotic factors that varied seasonally. I also found that the population consisted of individuals that displayed an extremely wide range of movement and feeding behaviors, indicating that individual specialization is potentially an important determinant of the varied roles of alligators in ecosystems. Ultimately, I found that assuming top predator populations consist of individuals that all behave in similar ways in terms of their feeding, movements, and potential roles in ecosystems is likely incorrect. As climate change and ecosystem restoration and conservation activities continue to affect top predator populations worldwide, individuals will likely respond in different and possibly unexpected ways.