Project Publications

Wing serial homologues and the diversification of insect outgrowths: insights from the pupae of scarab beetles (2021)

Wing serial homologues and the diversification of insect outgrowths: insights from the pupae of scarab beetles (2021)

Modification of serially homologous structures is a common avenue towards functional innovation in developmental evolution, yet ancestral affinities among serial homologues may be obscured as structure-specific modifications accumulate over time. We sought to assess the degree of homology to wings of three types of body wall projections commonly observed in scarab beetles: (i) the dorsomedial support structures found on the second and third thoracic segments of pupae, (ii) the abdominal support structures found bilaterally in most abdominal segments of pupae, and (iii) the pro-thoracic horns which depending on species and sex may be restricted to pupae or also found in adults. We functionally investigated 14 genes within, as well as two genes outside, the canonical wing gene regulatory net-work to compare and contrast their role in the formation of each of the three presumed wing serial homologues. We found 11 of 14 wing genes to be functionally required for the proper formation of lateral and dorsal support structures, respectively, and nine for the formation of prothoracic horns.At the same time, we document multiple instances of divergence in gene function across our focal structures. Collectively, our results support the hypothesis that dorsal and lateral support structures as well as prothoracic horns share a developmental origin with insect wings. Our findings suggest that the morphological and underlying gene regulatory diversification of wing serial homologues across species, life stages and segments has contributed significantly to the extraordinary diversity of arthropod appendages and outgrowths.

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From descent with modification to the origins of novelty (2021)

From descent with modification to the origins of novelty (2021)

Descent with modification is the foundational framework of all of evolution. Yet evolutionary novelties are defined as lacking affinities to structures that already existed in the ancestral state, i.e. to somehow emerge in the absence of homology. We posit that reconciling both perspectives necessitates the existence of a type of innovation gradient that allows descent with modification to seed the initiation of a novel trait, which once in existence can then diversify into its variant forms. Recent work on diverse, textbook examples of morphological novelties illustrate the value of the innovation gradient concept. Innovations as profound and diverse as insect wings, beetle horns, and treehopper helmets derive from homologous source tissues instructed in their development by homologous gene regulatory networks. Yet rather than rendering these traits no longer novel, we posit that discoveries such as these call for a reassessment of the usefulness of defining evolutionary novelty as necessitating the absence of homology. Instead, we need to redirect our attention to how ancestral homologies scaffold and bias the innovation gradient to facilitate hotspots of innovation in some places, and deep conservation elsewhere.

read more
Rapid differentiation of plasticity in life history and morphology during invasive range expansion and concurrent local adaptation in the horned beetle Onthophagus taurus (2020)

Rapid differentiation of plasticity in life history and morphology during invasive range expansion and concurrent local adaptation in the horned beetle Onthophagus taurus (2020)

Understanding the interplay between genetic differentiation, ancestral plasticity, and the evolution of plasticity during adaptation to environmental variation is critical to predict populations’ responses to environmental change. However, the role of plasticity in rapid adaptation in nature remains poorly understood. We here use the invasion of the horned beetle Onthophagus taurus in the United States during the last half century to study the contribution of ancestral plasticity and post-invasion evolution of plastic responses in rapid population differentiation. We document latitudinal variation in life history and morphology, including genetic compensation in development time and body size, likely adaptive responses to seasonal constraints in the North. However, clinal variation in development time and sizewas strongly dependent on rearing temperature, suggesting that population differentiation in plasticity played a critical role in successful adaptation on ecological timescales. Clinal variation in wing shape was independent of ancestral plasticity, but correlated with derived plasticity, consistent with evolutionary interdependence. In contrast, clinal variation
in tibia shape aligned poorly with thermal plasticity. Overall, this study suggests that post-invasion evolution of plasticity contributed to range expansions and concurrent adaptation to novel climatic conditions.

read more
Integrating evolutionarily novel hornswithin the deeply conserved insect head (2020)

Integrating evolutionarily novel hornswithin the deeply conserved insect head (2020)

How novel traits integrate within ancient trait complexes without compromising ancestral functions is a foundational challenge in evo-devo. The insect head represents an ancient body region patterned by a deeply conserved developmental genetic network, yet at the same time constitutes a hot spot for morphological innovation. However, the mechanisms that facilitate the repeated emergence, integration, and diversification of morphological novelties within this body region are virtually unknown. Using horned Onthophagus beetles, we investigated the mechanisms that instruct the development of the dorsal adult head and the formation and integration of head horns, one of the most elaborate classes of secondary sexual weapons in the animal kingdom.

read more
Nutrition-responsive gene expression and the developmental evolution of insect polyphenism (2020)

Nutrition-responsive gene expression and the developmental evolution of insect polyphenism (2020)

Nutrition-responsive development is a ubiquitous and highly diversified example of phenotypic plasticity, yet its underlying molecular and developmental mechanisms and modes of evolutionary diversification remain poorly understood. We measured genome-wide transcription in three closely related species of horned beetles exhibiting strikingly diverse degrees of nutrition responsiveness in the development of male weaponry. We show that (1) counts of differentially expressed genes between low- and high-nutritional backgrounds mirror species-specific degrees of morphological nutrition responsiveness; (2) evolutionary exaggeration of morphological responsiveness is underlain by both amplification of ancestral nutrition-responsive gene expres-sion and recruitment of formerly low nutritionally responsive genes; and (3) secondary loss of morphological responsiveness to nutrition coincides with a dramatic reduction in gene expression plasticity. Our results further implicate genetic accommoda-tion of ancestrally high variability of gene expression plasticity in both exaggeration and loss of nutritional plasticity, yet reject a major role of taxon-restricted genes in the developmental regulation and evolution of nutritional plasticity.

read more
Beetle horns evolved from wing serial homologs (2019)

Beetle horns evolved from wing serial homologs (2019)

Understanding how novel complex traits originate is a foundational challenge in evolutionary biology. We investigated the origin of prothoracic horns in scarabaeine beetles, one of the most pronounced examples of secondary sexual traits in the animal kingdom. We show that prothoracic horns derive from bilateral source tissues; that diverse wing genes are functionally required for instructing this process; and that, in the absence of Hox input, prothoracic horn primordia transform to contribute to ectopic wings.

read more

Project Publications

Wing serial homologues and the diversification of insect outgrowths: insights from the pupae of scarab beetles (2021)

Wing serial homologues and the diversification of insect outgrowths: insights from the pupae of scarab beetles (2021)

Modification of serially homologous structures is a common avenue towards functional innovation in developmental evolution, yet ancestral affinities among serial homologues may be obscured as structure-specific modifications accumulate over time. We sought to assess the degree of homology to wings of three types of body wall projections commonly observed in scarab beetles: (i) the dorsomedial support structures found on the second and third thoracic segments of pupae, (ii) the abdominal support structures found bilaterally in most abdominal segments of pupae, and (iii) the pro-thoracic horns which depending on species and sex may be restricted to pupae or also found in adults. We functionally investigated 14 genes within, as well as two genes outside, the canonical wing gene regulatory net-work to compare and contrast their role in the formation of each of the three presumed wing serial homologues. We found 11 of 14 wing genes to be functionally required for the proper formation of lateral and dorsal support structures, respectively, and nine for the formation of prothoracic horns.At the same time, we document multiple instances of divergence in gene function across our focal structures. Collectively, our results support the hypothesis that dorsal and lateral support structures as well as prothoracic horns share a developmental origin with insect wings. Our findings suggest that the morphological and underlying gene regulatory diversification of wing serial homologues across species, life stages and segments has contributed significantly to the extraordinary diversity of arthropod appendages and outgrowths.

read more
From descent with modification to the origins of novelty (2021)

From descent with modification to the origins of novelty (2021)

Descent with modification is the foundational framework of all of evolution. Yet evolutionary novelties are defined as lacking affinities to structures that already existed in the ancestral state, i.e. to somehow emerge in the absence of homology. We posit that reconciling both perspectives necessitates the existence of a type of innovation gradient that allows descent with modification to seed the initiation of a novel trait, which once in existence can then diversify into its variant forms. Recent work on diverse, textbook examples of morphological novelties illustrate the value of the innovation gradient concept. Innovations as profound and diverse as insect wings, beetle horns, and treehopper helmets derive from homologous source tissues instructed in their development by homologous gene regulatory networks. Yet rather than rendering these traits no longer novel, we posit that discoveries such as these call for a reassessment of the usefulness of defining evolutionary novelty as necessitating the absence of homology. Instead, we need to redirect our attention to how ancestral homologies scaffold and bias the innovation gradient to facilitate hotspots of innovation in some places, and deep conservation elsewhere.

read more
Rapid differentiation of plasticity in life history and morphology during invasive range expansion and concurrent local adaptation in the horned beetle Onthophagus taurus (2020)

Rapid differentiation of plasticity in life history and morphology during invasive range expansion and concurrent local adaptation in the horned beetle Onthophagus taurus (2020)

Understanding the interplay between genetic differentiation, ancestral plasticity, and the evolution of plasticity during adaptation to environmental variation is critical to predict populations’ responses to environmental change. However, the role of plasticity in rapid adaptation in nature remains poorly understood. We here use the invasion of the horned beetle Onthophagus taurus in the United States during the last half century to study the contribution of ancestral plasticity and post-invasion evolution of plastic responses in rapid population differentiation. We document latitudinal variation in life history and morphology, including genetic compensation in development time and body size, likely adaptive responses to seasonal constraints in the North. However, clinal variation in development time and sizewas strongly dependent on rearing temperature, suggesting that population differentiation in plasticity played a critical role in successful adaptation on ecological timescales. Clinal variation in wing shape was independent of ancestral plasticity, but correlated with derived plasticity, consistent with evolutionary interdependence. In contrast, clinal variation
in tibia shape aligned poorly with thermal plasticity. Overall, this study suggests that post-invasion evolution of plasticity contributed to range expansions and concurrent adaptation to novel climatic conditions.

read more
Integrating evolutionarily novel hornswithin the deeply conserved insect head (2020)

Integrating evolutionarily novel hornswithin the deeply conserved insect head (2020)

How novel traits integrate within ancient trait complexes without compromising ancestral functions is a foundational challenge in evo-devo. The insect head represents an ancient body region patterned by a deeply conserved developmental genetic network, yet at the same time constitutes a hot spot for morphological innovation. However, the mechanisms that facilitate the repeated emergence, integration, and diversification of morphological novelties within this body region are virtually unknown. Using horned Onthophagus beetles, we investigated the mechanisms that instruct the development of the dorsal adult head and the formation and integration of head horns, one of the most elaborate classes of secondary sexual weapons in the animal kingdom.

read more
Nutrition-responsive gene expression and the developmental evolution of insect polyphenism (2020)

Nutrition-responsive gene expression and the developmental evolution of insect polyphenism (2020)

Nutrition-responsive development is a ubiquitous and highly diversified example of phenotypic plasticity, yet its underlying molecular and developmental mechanisms and modes of evolutionary diversification remain poorly understood. We measured genome-wide transcription in three closely related species of horned beetles exhibiting strikingly diverse degrees of nutrition responsiveness in the development of male weaponry. We show that (1) counts of differentially expressed genes between low- and high-nutritional backgrounds mirror species-specific degrees of morphological nutrition responsiveness; (2) evolutionary exaggeration of morphological responsiveness is underlain by both amplification of ancestral nutrition-responsive gene expres-sion and recruitment of formerly low nutritionally responsive genes; and (3) secondary loss of morphological responsiveness to nutrition coincides with a dramatic reduction in gene expression plasticity. Our results further implicate genetic accommoda-tion of ancestrally high variability of gene expression plasticity in both exaggeration and loss of nutritional plasticity, yet reject a major role of taxon-restricted genes in the developmental regulation and evolution of nutritional plasticity.

read more
Beetle horns evolved from wing serial homologs (2019)

Beetle horns evolved from wing serial homologs (2019)

Understanding how novel complex traits originate is a foundational challenge in evolutionary biology. We investigated the origin of prothoracic horns in scarabaeine beetles, one of the most pronounced examples of secondary sexual traits in the animal kingdom. We show that prothoracic horns derive from bilateral source tissues; that diverse wing genes are functionally required for instructing this process; and that, in the absence of Hox input, prothoracic horn primordia transform to contribute to ectopic wings.

read more

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© 2020 Agency in Living Systems

© 2020 Agency in Living Systems