Selection against Accumulating Mutations in Niche-Preference Genes Can Drive Speciation

Our current understanding of sympatric speciation is that it occurs primarily through disruptive selection on ecological genes driven by competition, followed by reproductive isolation through reinforcement-like selection against inferior intermediates/heterozygotes. Our evolutionary model of selection on resource recognition and preference traits suggests a new mechanism for sympatric speciation. We find speciation can occur in three phases. First a polymorphism of functionally different phenotypes is established through evolution of specialization. On the gene level, regulatory functions have evolved in which some alleles are conditionally switched off (i.e. are silent). These alleles accumulate harmful mutations that potentially may be expressed in offspring through recombination. Second mating associated with resource preference invades because harmful mutations in parents are not expressed in the offspring when mating assortatively, thereby dividing the population into two pre-zygotically isolated resource-specialist lineages. Third, silent alleles that evolved in phase one now accumulate deleterious mutations over the following generations in a Bateson-Dobzhansky-Muller fashion, establishing a post-zygotic barrier to hybridization

The evolution of niche width

PhD ThesisThis thesis examines the ultimate and proximate determinants of niche width, with a focus on how cognition and biological information processing may drive the evolution of niche width. Using both field and laboratory experiments I investigate how learning can alter resource use in syrphids. Modelling biological information processing using artificial neural networks I consider how various ecological factors interact and can impact information processing to determine decision accuracy (a proposed factor in the evolution of niche width). Finally the ability of artificial neural networks to overcome evolutionary dead ends due to specialisation and functional loss is examined. I found that syrphids were able to use external, inter-specific cues to alter their resource use. Specialist artificial neural networks decision accuracy was altered by the introduction of the ecological variables they were subjected to and the loss of functionality can create an evolutionary dead end scenario only in very extreme cases or under specific ecological pressures. I studied the syrphid (Episyrphus balteatus) both in the field and under laboratory conditions. There is a huge amount of literature describing how bees use scent marks to aid decision making before landing on flowers but there is currently no work on the syrphids ability to detect and utilise these scent marks. The question I posed was ‘Can syrphids modify their pattern of resource utilisation by using this scent mark information?’ The field work was carried out using motion detection cameras positioned above flowers of knapweed (Centaurea nigra). The flowers had two different treatments: one was bagged overnight to prevent pollinator access and the other was left unbagged allowing foraging insects to deplete the nectar and pollen. Visits from both conditions were recorded and compared. I found that previously bagged flowers received more visits from both bumblebees (Bombus spp.) and syrphids suggesting that syrphids could also detect when a flower was depleted without landing. iii The laboratory tests were conducted in an arena using artificial flowers. The experiment was split into a learning phase and a testing phase. I tested the syrphids ability to recognise and learn an association to two different compounds, bee scent marks or 1-Hexanol. I found that syrphids could learn to associate both bee scent marks and 1-Hexanol with negative rewards and use this information to change their foraging behaviour. I used artificial neural networks to investigate differences between the decision accuracy of specialists and generalists when foraging under ecological pressures. Previous work has shown that specialists had higher decision accuracy when non-host selection carried a mild reward and I was interested to see how ecological variables would impact this advantage. The ecological conditions I considered were search costs, resource availability and starvation. To do this I trained neural networks to recognise different numbers of binary images (hosts) over a range of positive and negative non-host rewards or punishments. The fewer hosts a network had the more specialised it was. I found that both starvation and resource availability reduced the range of non-host values across which specialist networks had a fitness advantage over generalists. Interestingly I found that introducing search costs shifts the range of non-host values where specialist advantage occurs rather than narrowing them as in the previous conditions. Specialists suffering from search costs performed better when non-host selection carried a high to intermediate punishment. Finally, I used artificial neural networks to investigate the evolutionary dead end theory. This theory states that specialist organisms will lose genetic variation and will be unable to respond as effectively to ecological change. I first trained networks as specialists. These networks were then re-trained as generalists. While re-training networks had a percentage of their weights fixed to simulate the suggested reduction in evolutionary potential of specialists. Ecological conditions in these simulations were either non-host penalties, search costs or a combination of the two. I found that networks were relatively robust to loss of evolutionary iv potential. All of the networks performed well even at intermediate (50%) weight fixation. The application of search costs reduced overall network fitness but this effect was not as pronounced as when non-host penalties were introduced. Non-host penalties had the greatest effect on the fitness of networks. These results suggest that specialisation should only become an ‘evolutionary dead end’ under very specific and severe conditions.Natural Environment Research Council (NERC

Patterns of visual adaptation in tropical mimetic butterflies

Species diversity within an ecosystem can be supported by favouring microhabitat specialisation. In complex habitats, like tropical rainforests, spatial and temporal segregation across microhabitats can expose species to distinct sensory realms. For many animals, visual systems serve as the primary conduit for perceiving biologically relevant sensory information, and the structural and functional variety of eyes and sensory brain regions reflects their critical role in diverse animal behaviours. However, little is known of their role in mediating niche segregation across subtle ecological scales, particularly in terrestrial environments. I explore the role of microhabitat partitioning in driving predictable patterns of adaptive visual system evolution within two diverse radiations of mimetic Neotropical butterfly, the Heliconius and Ithomiini. By taking a comparative approach, I investigate whether dual patterns of habitat divergence and convergence is manifested in the visual system at the perceptual, processing, and molecular level. I find extensive evidence of heritable, habitat-associated visual system variation, particularly for neural processing structures, hinting at the evolutionary lability of these systems to rapidly accommodate local adaptations to visual ecologies. My research also empirically demonstrates, for the first time, how variation in forest structure can give rise to distinct photic environments, highlighting the role of spectral variation as a major driver of adaptive community assemblage within a terrestrial forest radiation. In addition, evidence of visual morphological convergence offers a mechanistic insight into the evolvability of visual adaptations when confronted with similar ecological challenges, shedding light on their significance in promoting ecological diversification and speciation

Roadmap on biology in time varying environments

Biological organisms experience constantly changing environments, from sudden changes in physiology brought about by feeding, to the regular rising and setting of the Sun, to ecological changes over evolutionary timescales. Living organisms have evolved to thrive in this changing world but the general principles by which organisms shape and are shaped by time varying environments remain elusive. Our understanding is particularly poor in the intermediate regime with no separation of timescales, where the environment changes on the same timescale as the physiological or evolutionary response. Experiments to systematically characterize the response to dynamic environments are challenging since such environments are inherently high dimensional. This roadmap deals with the unique role played by time varying environments in biological phenomena across scales, from physiology to evolution, seeking to emphasize the commonalities and the challenges faced in this emerging area of research

When and Why Did Human Brains Decrease in Size? A New Change-Point Analysis and Insights From Brain Evolution in Ants

Human brain size nearly quadrupled in the six million years since Homo last shared a common ancestor with chimpanzees, but human brains are thought to have decreased in volume since the end of the last Ice Age. The timing and reason for this decrease is enigmatic. Here we use change-point analysis to estimate the timing of changes in the rate of hominin brain evolution. We find that hominin brains experienced positive rate changes at 2.1 and 1.5 million years ago, coincident with the early evolution of Homo and technological innovations evident in the archeological record. But we also find that human brain size reduction was surprisingly recent, occurring in the last 3,000 years. Our dating does not support hypotheses concerning brain size reduction as a by-product of body size reduction, a result of a shift to an agricultural diet, or a consequence of self-domestication. We suggest our analysis supports the hypothesis that the recent decrease in brain size may instead result from the externalization of knowledge and advantages of group-level decision-making due in part to the advent of social systems of distributed cognition and the storage and sharing of information. Humans live in social groups in which multiple brains contribute to the emergence of collective intelligence. Although difficult to study in the deep history of Homo, the impacts of group size, social organization, collective intelligence and other potential selective forces on brain evolution can be elucidated using ants as models. The remarkable ecological diversity of ants and their species richness encompasses forms convergent in aspects of human sociality, including large group size, agrarian life histories, division of labor, and collective cognition. Ants provide a wide range of social systems to generate and test hypotheses concerning brain size enlargement or reduction and aid in interpreting patterns of brain evolution identified in humans. Although humans and ants represent very different routes in social and cognitive evolution, the insights ants offer can broadly inform us of the selective forces that influence brain size

Chemosensory receptors in the tobacco hawkmoth Manduca sexta

Chemosensation, the sense of smell and taste, allows animals to assess the chemical properties of their environment. They use it to identify food sources, avoid harmful substances, find mating partners, escape from predators and to find places suitable for their offspring. We employed the tobacco hawkmoth Manduca sexta (Lepidoptera: Sphingidae) to study the molecular basis of chemosensation in the context of the insect’s environment. Therefore, we generated RNAseq data sets of several chemosenory tissues in several physiological states of M. sexta. We used this data to correct the gene models generated by an automated annotation pipeline as part of the M. sexta genome project to build a reference set of chemosensory receptor genes. This gene set will facilitate future Lepidoptera genome projects. We used the corrected and several new gene models to find sex specifically expressed genes and to characterize the chemosensory repertoire of larvae. Thus, I could formulate hypotheses about their role in the life of female and male moths as well as larvae. We report expression of chemosensory receptors in the ovipositor. Furthermore, we identified putative olfactory sensilla on the ovipositor and using electrophysiological recording we identified ligands which could be important for oviposition site selection. In a third study, we challenged M. sexta larvae by rearing them on host and non- host plants. We checked the expression of detoxification, immune system related and chemosensory genes to assess the ability of M. sexta larvae to adapt to their environment. This thesis provides insights into the molecular basis of chemosensation in different ecological contexts, following the life cycle of a lepidopteran species from mating and oviposition throughout the larval stage. The principles studied here in M. sexta can be applied and generalized to other insects and will facilitate further research in chemica

Schopnost diskriminace květních morfotypů u pestřenek

Atraktivita květů pro opylovače je zprostředkována několika květními znaky. Schopnost rozlišovat květiny na základě těchto květních vlastností je velmi důležitá pro reprodukci květin a výživu a následně i reprodukci opylovačů. Na modelovém organismu Eristalis tenax jsme v laboratorních podmínkách testovali tři květní znaky - barvu, velikost a tvar a jejich kombinace na umělých květech vytištěných na 3D tiskárně. Zjistili jsme, že nejdůležitějším květním znakem byla barva následovaná velikostí a že efekt barvy byl zesílen efektem velikosti, ale pouze u preferované barvy. To naznačuje, že preference pro květinové vlastnosti jsou nějakým způsobem strukturované. Vliv symetrie jsme nenašli. Následně jsme v terénu pozorovali nenaivní pestřenky a čmeláky na jednodruhové patchi rostliny čertkusu lučního (Succisa pratensis). Zajímala nás role ostatních květních znaků v momentě, kdy se barva a velikost neliší. Nejdůležitějšími charakteristikami potom byla výška a efektivní počet kvítků v květenství. Pestřenky měly obecně delší návštěvy než čmeláci a navštěvovaly více květů. Na druhou stranu čmeláci dělali kratší a efektivnější návštěvy, což pravděpodobně souvisí s jejich eusocialitou. Klíčová slova: Syrphidae, Apidae, Eristalis tenax, Bombus spp., symetrie květu, velikost květu, barva květu, opylováníThe attractiveness of flowers to pollinators is mediated by several floral traits. The ability to discriminate the flowers based on these floral traits is crucial for the flower reproduction and pollinator nutrition and reproduction. We tested three floral traits - colour, size and shape - along with their combinations using artificially 3D printed flowers on model organism Eristalis tenax in laboratory conditions. Our findings revealed that the most important floral trait was the colour followed by size. Additionally, the effect of colour was enhanced by size, but only for the preferred colour. This suggests that preferences for specific floral traits can be structured. The effect of symmetry was not significant. Subsequently, we observed non-naïve hoverflies and bumblebees in the field on flower patch consisting of devil's-bit scabious (Succisa pratensis). We were interested in the role of other floral traits when the colour and size were indistinguishable. The most important characteristics were height and effective number of florets in the inflorescence. The hoverflies tend to do longer visits than bumblebees and visited more flowers as well. Conversely, bumblebees did shorter but more efficient visits, likely due to their eusociality. Keywords: Syrphidae, Apidae, Eristalis tenax, Bombus spp.,...Katedra zoologieDepartment of ZoologyPřírodovědecká fakultaFaculty of Scienc

Neuroecology of social organization in the Australasian weaver ant, Oecophylla smaragdina

The social brain hypothesis predicts that larger group size and greater social complexity select for increased brain size. In ants, social complexity is associated with large colony size, emergent collective action, and division of labor among workers. The great diversity of social organization in ants offers numerous systems to test social brain theory and examine the neurobiology of social behavior. My studies focused on the Australasian weaver ant, Oecophylla smaragdina, a polymorphic species, as a model of advanced social organization. I critically analyzed how biogenic amines modulate social behavior in ants and examined their role in worker subcaste-related territorial aggression. Major workers that naturally engage in territorial defense showed higher levels of brain octopamine in comparison to more docile, smaller minor workers, whose social role is nursing. Through pharmacological manipulations of octopaminergic action in both subcastes, octopamine was found to be both necessary and sufficient for aggression, suggesting subcaste-related task specialization results from neuromodulation. Additionally, I tested social brain theory by contrasting the neurobiological correlates of social organization in a phylogenetically closely related ant species, Formica subsericea, which is more basic in social structure. Specifically, I compared brain neuroanatomy and neurometabolism in respect to the neuroecology and degree of social complexity of O. smaragdina major and minor workers and F. subsericea monomorphic workers. Increased brain production costs were found in both O. smaragdina subcastes, and the collective action of O. smaragdina majors appeared to compensate for these elevated costs through decreased ATP usage, measured from cytochrome oxidase activity, an endogenous marker of neurometabolism. Macroscopic and cellular neuroanatomical analyses of brain development showed that higher-order sensory processing regions in workers of O. smaragdina, but not F. subsericea, had age-related synaptic reorganization and increased volume. Supporting the social brain hypothesis, ecological and social challenges associated with large colony size were found to contribute to increased brain size. I conclude that division of labor and collective action, among other components of social complexity, may drive the evolution of brain structure and function in compensatory ways by generating anatomically and metabolically plastic mosaic brains that adaptively reflect cognitive demands of worker task specialization and colony-level social organization

CONSTRAINTS OF THE IMAGINATION: HOW PHENOTYPES ARE SHAPED THROUGH GENETICS, THE ENVIRONMENT, AND DEVELOPMENT

Phenotypic constraints are ubiquitous throughout nature, being found throughout all stages of life and at multiple different biological levels including cellular, genetic, environmental, behavioral, evolutionary, and developmental. These constraints have shaped, not only the natural world, but the way that we perceive what is possible, or impossible, an observation made clear by François Jacob in his 1977 paper “Evolution and Tinkering”. This is reflected in the literature, repeatedly, by the regular occurrence of densely packed visualization of phenotypic space that seemingly always have large areas that go unoccupied. Despite constrained regions of space being observable across countless taxa, identifying the mechanisms of those constraints remains elusive. Given that constraints are widespread and have influenced how evolution may work, my aim was to identify mechanisms of constraint throughout multiple biological levels. Chapter one is divided into two parts, sections A and B, but largely focuses on how constraints are influenced by genetics. For this, we investigated crocc2, a protein that encodes for a structural component of the ciliary rootlet which in turn plays a major role as a mechanosensory for nearly all cells. We found dysfunctional crocc2 resulted in both dysmorphic bone development and a decrease in the plastic response potential of zebrafish (section A), as well as altered developmental trajectories in juvenile morphology, presumably due to alterations in cellular polarity and inadequate extracellular communication. Importantly, all results from this chapter point toward crocc2 play a canalizing role in the production of phenotypes at multiple life-history stages. Chapter 2 takes a different approach into understanding constrains by looking at broad ecological alterations and how those alterations may alter morphology of resident taxa. Here, we utilized the heavily altered habitat of the Tocantins River in the Amazon and the existing museum collections to evaluate how select representatives of the cichlid community had responded to such change. We found significant changes in contemporary morphology across all included cichlid species compared to their historical counterparts. These data show that alterations to the environment have resulted in changes to the local resident species, and possibly an alteration to their future evolutionary trajectories. Among the species included, one was found to have the most substantial morphological changes, which is what we followed up in the next chapter. Chapter 3 dug into the morphological changes of Satanoperca, a Geophagine cichlid with a unique feeding mechanism known as winnowing. Winnowing is a poorly understood mechanical process involving substrate manipulation. Given that anthropogenic alterations to local hydrology oft result in changes to the benthic sediment composition, we wanted to know if differing substrates was enough to induce a plastic response in winnowing fishes, and if so which traits were effected. We found significant differences across our experimental populations in both shape and disparity and present evidence in support of wide-spread integration across craniofacial traits. In addition, these data suggest that the novel anatomical structure, the epibranchial lobe, is more modular than other craniofacial traits involved in the winnowing process. Chapters 4 and 5 utilize a unique lineage of fishes, the Bramidae, to understand how developmental and evolutionary constraints are broken to produce morphological novelties. We used a combination of DNA sequences from GenBank and numerous museum specimens to illuminate constraints and determine how constraints are broken to produce complex phenotypic novelties. In Chapter 4, we found that the fanfishes had experienced greater rates of morphological evolution than other members of the Bramidae family, resulting in their occupation of an entirely novel region of phenotypic space. In Chapter 5, we elaborated on this by investigating the developmental processes involved in producing an extreme morphological novelty. The data presented in Chapter 5 provide evidence suggesting that the fanfishes have broken various constraints, resulting in prominent anatomical and morphological changes to accommodate their novel phenotype. In all, my dissertation provides examples of how constraints have shaped the variability that we see throughout life and shows examples of how constraints can be identified, what happens when they are broken, and how they work to control the pace and trajectory of evolutionary processes