The role of plasticity in evolution across scales:
from gene function to global intra- and interspecific diversification
I am broadly interested in the ultimate and proximate underpinnings of the stunning diversity of organismal shapes, sizes, and lifestyles. This applies in particular to the mechanisms driving rapid diversification of morphology, behavior, and life history in insects. Specifically, my research integrates quantitative and functional genetic, experimental, and comparative approaches to uncover how phenotypic plasticity arises and, once in existence, shapes subsequent evolutionary change.
from gene function to global intra- and interspecific diversification
I am broadly interested in the ultimate and proximate underpinnings of the stunning diversity of organismal shapes, sizes, and lifestyles. This applies in particular to the mechanisms driving rapid diversification of morphology, behavior, and life history in insects. Specifically, my research integrates quantitative and functional genetic, experimental, and comparative approaches to uncover how phenotypic plasticity arises and, once in existence, shapes subsequent evolutionary change.
Evolutionary ecology of sexual dimorphism
During my undergraduate and early graduate work with Wolf Blanckenhorn at the University of Zurich, my interests in natural history sparked a deep curiosity about the evolutionary processes fueling phenotypic variation. This motivated me to study the role of natural and sexual selection in driving intraspecific population differentiation in sexual size dimorphism in sepsid flies. Using a classic evolutionary ecological framework, this early work demonstrated that variation in the strength of sexual selection accounts for the convergent evolution of male-biased sexual size dimorphism both within and among lineages (Rohner et al. 2016 Evolution). Combined with several follow-up studies (Baur et al. 2019 Journal of Evolutionary Biology; Blanckenhorn et al. 2020 Oikos, Animal Behaviour), this allowed me to link mating system variation to sexual dimorphism in behavior and morphology. However, while this line of research uncovered the ultimate underpinnings of phenotypic diversity, I realized that sexual dimorphism is strongly dependent on environmental conditions. This realization motivated my subsequent dissertation research interests in the evolution of sex-specific plasticity. This body of work, which was awarded the Alfred Russel Wallace Award 2018 of the Royal Entomological Society, investigated the causes and consequences of life history plasticity and its evolution in insects. It allowed me to document the crucial role of sex-specific plasticity in generating variation in sexual dimorphism not only among populations of sepsids, but also in generating interspecific variation in several species of other Diptera and even across all holometabolous insects (Fig. 1; Rohner et al. 2018 Functional Ecology; Rohner & Blanckenhorn 2018 American Naturalist). Detailed laboratory experiments further revealed the physiological mechanisms generating sexual size dimorphism in the yellow dung fly and again suggested that sex-specific plasticity of critical physiological aspects of insect growth plays a major role in generating and shaping variation in sexual size dimorphism and sex-specific plasticity (Rohner et al. 2017 Evolution & Development).
During my undergraduate and early graduate work with Wolf Blanckenhorn at the University of Zurich, my interests in natural history sparked a deep curiosity about the evolutionary processes fueling phenotypic variation. This motivated me to study the role of natural and sexual selection in driving intraspecific population differentiation in sexual size dimorphism in sepsid flies. Using a classic evolutionary ecological framework, this early work demonstrated that variation in the strength of sexual selection accounts for the convergent evolution of male-biased sexual size dimorphism both within and among lineages (Rohner et al. 2016 Evolution). Combined with several follow-up studies (Baur et al. 2019 Journal of Evolutionary Biology; Blanckenhorn et al. 2020 Oikos, Animal Behaviour), this allowed me to link mating system variation to sexual dimorphism in behavior and morphology. However, while this line of research uncovered the ultimate underpinnings of phenotypic diversity, I realized that sexual dimorphism is strongly dependent on environmental conditions. This realization motivated my subsequent dissertation research interests in the evolution of sex-specific plasticity. This body of work, which was awarded the Alfred Russel Wallace Award 2018 of the Royal Entomological Society, investigated the causes and consequences of life history plasticity and its evolution in insects. It allowed me to document the crucial role of sex-specific plasticity in generating variation in sexual dimorphism not only among populations of sepsids, but also in generating interspecific variation in several species of other Diptera and even across all holometabolous insects (Fig. 1; Rohner et al. 2018 Functional Ecology; Rohner & Blanckenhorn 2018 American Naturalist). Detailed laboratory experiments further revealed the physiological mechanisms generating sexual size dimorphism in the yellow dung fly and again suggested that sex-specific plasticity of critical physiological aspects of insect growth plays a major role in generating and shaping variation in sexual size dimorphism and sex-specific plasticity (Rohner et al. 2017 Evolution & Development).
Functional genetic underpinnings of sex-specific plasticity in size and shape
In linking behavior, ecology, and physiology to the evolution of sex-specific plasticity, my graduate work advanced our understanding of why and how life history traits diverge among lineages. However, I also realized that my work lacked an understanding of the genetic and developmental basis of phenotypic variation. With an Early Postdoc.Mobility Fellowship of the Swiss National Science Foundation, I took the opportunity to pursue postdoctoral research with Prof. Armin Moczek (Indiana University, USA) to study the developmental/genetic basis of sex-specific plasticity. Ongoing work integrates geometric morphometrics, transcriptomics (RNA sequencing), and functional genetics (RNA interference). Combining these approaches, I have been able to demonstrate that the highly conserved somatic sex determination gene doublesex (dsx) and its sex-specific isoforms function as master regulators of sex-specific plasticity (Fig. 2). Gene knockdowns in several species reveal that the evolution of heightened nutritional plasticity in males is mediated by rapid evolution of dsx function. This evolutionarily conserved mechanism thus enables the resolution of intralocus conflict arising from environment-dependent antagonistic selection among sexes via sex-specific expression of alternatively spliced dsx isoforms and provides a molecular mechanism facilitating sex-specific plasticity and its evolution. These findings also suggest that sex-specific alternative splicing of dsx mediates the resolution of intralocus conflict and thus has major implications for our conceptual understanding of how genetic correlations between sexes, environments, and traits can be overcome.
In linking behavior, ecology, and physiology to the evolution of sex-specific plasticity, my graduate work advanced our understanding of why and how life history traits diverge among lineages. However, I also realized that my work lacked an understanding of the genetic and developmental basis of phenotypic variation. With an Early Postdoc.Mobility Fellowship of the Swiss National Science Foundation, I took the opportunity to pursue postdoctoral research with Prof. Armin Moczek (Indiana University, USA) to study the developmental/genetic basis of sex-specific plasticity. Ongoing work integrates geometric morphometrics, transcriptomics (RNA sequencing), and functional genetics (RNA interference). Combining these approaches, I have been able to demonstrate that the highly conserved somatic sex determination gene doublesex (dsx) and its sex-specific isoforms function as master regulators of sex-specific plasticity (Fig. 2). Gene knockdowns in several species reveal that the evolution of heightened nutritional plasticity in males is mediated by rapid evolution of dsx function. This evolutionarily conserved mechanism thus enables the resolution of intralocus conflict arising from environment-dependent antagonistic selection among sexes via sex-specific expression of alternatively spliced dsx isoforms and provides a molecular mechanism facilitating sex-specific plasticity and its evolution. These findings also suggest that sex-specific alternative splicing of dsx mediates the resolution of intralocus conflict and thus has major implications for our conceptual understanding of how genetic correlations between sexes, environments, and traits can be overcome.
Thermal plasticity and its relationship to local adaptation
The role of plasticity of life history and complex morphological traits during local adaptation to climatic variation represents a further core focus of my research. I investigated interspecific patterns of several life-history traits in 150 species of fruit flies (Rohner et al. 2018 Ecography), quantitative genetic population differentiation across three continents in the yellow dung fly (Schäfer et al 2018 Evolution) and several species of black scavenger flies (Roy et al. 2018 Oecologia; Rohner et al. 2019 Journal of Evolutionary Biology). Together, these studies highlight the importance of plasticity in population differentiation across large geographic gradients. My postdoctoral work further extends this work by demonstrating how the evolution of developmental plasticity itself plays critical roles in rapid adaptation to environmental conditions in an invasive dung beetle (Fig. 3; Rohner & Moczek 2020 Evolution). Taken together, my work shows that thermal plasticity is often related to local adaptation to climate, and that plastic responses and their magnitude can impact a species’ response even on ‘ecological’ timescales.
The role of plasticity of life history and complex morphological traits during local adaptation to climatic variation represents a further core focus of my research. I investigated interspecific patterns of several life-history traits in 150 species of fruit flies (Rohner et al. 2018 Ecography), quantitative genetic population differentiation across three continents in the yellow dung fly (Schäfer et al 2018 Evolution) and several species of black scavenger flies (Roy et al. 2018 Oecologia; Rohner et al. 2019 Journal of Evolutionary Biology). Together, these studies highlight the importance of plasticity in population differentiation across large geographic gradients. My postdoctoral work further extends this work by demonstrating how the evolution of developmental plasticity itself plays critical roles in rapid adaptation to environmental conditions in an invasive dung beetle (Fig. 3; Rohner & Moczek 2020 Evolution). Taken together, my work shows that thermal plasticity is often related to local adaptation to climate, and that plastic responses and their magnitude can impact a species’ response even on ‘ecological’ timescales.
Evolution and development of complex morphological structures and their scaling
A further cornerstone of my research is the role of selection and developmental plasticity in the evolution of the shape of complex morphological structures (Rohner et al. Ecology & Evolution 2020; Baur et al. 2020 Journal of Evolutionary Biology). For instance, applying a comparative geometric morphometric framework, my research demonstrates that despite vastly different ecologies, even distantly related fly species maintained very similar wing shape allometries. Furthermore, allometric shape changes within a single population predict evolutionary diversification that unfolded in the higher Diptera throughout the Cenozoic. This suggests the existence of mechanisms that canalize variation or limit divergence in allometry of complex trait for over 65 million years, yet the nature of such mechanisms remain poorly understood (Rohner 2020 Journal of Evolutionary Biology). Ongoing research in dung beetle horns and fly wings starts to address the developmental genetic underpinnings of the evolution of shape. This includes the role of Notch signaling in morph-specific allometry (Crabtree et al. 2020 Development Genes and Evolution), and the function of sex determination, insulin, and Hedgehog signaling pathways in the evolutionary divergence in horn size and shape across dung beetle populations (Fig. 4; Rohner et al. unpublished data).
A further cornerstone of my research is the role of selection and developmental plasticity in the evolution of the shape of complex morphological structures (Rohner et al. Ecology & Evolution 2020; Baur et al. 2020 Journal of Evolutionary Biology). For instance, applying a comparative geometric morphometric framework, my research demonstrates that despite vastly different ecologies, even distantly related fly species maintained very similar wing shape allometries. Furthermore, allometric shape changes within a single population predict evolutionary diversification that unfolded in the higher Diptera throughout the Cenozoic. This suggests the existence of mechanisms that canalize variation or limit divergence in allometry of complex trait for over 65 million years, yet the nature of such mechanisms remain poorly understood (Rohner 2020 Journal of Evolutionary Biology). Ongoing research in dung beetle horns and fly wings starts to address the developmental genetic underpinnings of the evolution of shape. This includes the role of Notch signaling in morph-specific allometry (Crabtree et al. 2020 Development Genes and Evolution), and the function of sex determination, insulin, and Hedgehog signaling pathways in the evolutionary divergence in horn size and shape across dung beetle populations (Fig. 4; Rohner et al. unpublished data).
Outlook
Integrating a wide range of analytical approaches, including geometric morphometrics, transcriptomics, and quantitative as well as functional genetics, my research is situated at the interface between classic evolutionary and ecological research, behavior, and developmental genetics. Studying plasticity at different levels of organization —from gene function and physiology to intra- and interspecific diversification— revealed complex yet ubiquitous impacts of plasticity on adaptive evolution and provides a framework to explore how developmental systems and ecological circumstances interact with selection to shape evolutionary change. My future research will further strengthen this integrative research program by exploring the role of host-endosymbiont interactions and niche construction in the evolution and plasticity of life histories, and by studying to what extent selection on developmental plasticity biases the effects of future mutations. Taken together, my current and planned research program thus links phenotypic diversity to its proximate and ultimate causes, thereby furthering our understanding of why and how organismal form and function evolve the way they do.
Integrating a wide range of analytical approaches, including geometric morphometrics, transcriptomics, and quantitative as well as functional genetics, my research is situated at the interface between classic evolutionary and ecological research, behavior, and developmental genetics. Studying plasticity at different levels of organization —from gene function and physiology to intra- and interspecific diversification— revealed complex yet ubiquitous impacts of plasticity on adaptive evolution and provides a framework to explore how developmental systems and ecological circumstances interact with selection to shape evolutionary change. My future research will further strengthen this integrative research program by exploring the role of host-endosymbiont interactions and niche construction in the evolution and plasticity of life histories, and by studying to what extent selection on developmental plasticity biases the effects of future mutations. Taken together, my current and planned research program thus links phenotypic diversity to its proximate and ultimate causes, thereby furthering our understanding of why and how organismal form and function evolve the way they do.
