Many animals use tusks, spurs, antlers, and spines to get members of the same sex out of the way so that it becomes possible to get near members of the other sex. The sizes and shapes of such sexually selected weapons are stunningly diverse across taxa as well as within closely related groups. For example, the African antelope have many kinds of horns: some species have tiny spikes while others have large twisting and curving horns that may be pointing up, down, outwards, or inwards. Understanding why weapons are so diverse requires considering their function. Sexually selected weapons have evolved, at least in part, to function in physical combat.
We use experimentation to understand the evolution of weapon size, shape, and function within species, and we use phylogenetic comparative analyses to understand cumulative changes in weapons across species. Ultimately, our interest is on the evolutionary interplay of morphology and behaviour, and weapons and physical combat provide an outstanding opportunity to understand this interaction.
We test our hypotheses in two study systems. Our long-standing study system is the superfamily of insects called the leaf-footed bugs. This group includes ~3,300 species in five extant families, and it is one of only a few animal groups that produce weapons on the hind legs. In some of these species the hind legs exhibit extreme modifications including robust spines, club-like expansions, flags, and serrations. The diversity of their hind leg shapes, their ecology, and their behaviours provide outstanding opportunities for our work. We have recently started working with the sagebrush grig, Cyphoderris strepitans, in Grand Teton National Park. Insects in this genus offer a remarkable window into sexual selection and conflict. Females choose males partly by their song, then chew on their bodies and drink their haemolymph. Males hold females in place with a specialised weapon during sperm transfer. Both sexes mate multiply, but males become weaker and less attractive after mating, losing up to 10% of their body weight in a single encounter. This extraordinary system raises fundamental questions about how conflicting reproductive interests shape behaviour and morphology.
We currently have several projects focused on how seasonally changing plant environments influence male-male competition, signalling, weapon evolution, and the evolution of sexual dimorphism. With grant funding from the National Science Foundation, our team is examining how changes in host plants affect the growth and development of animal weapons and fighting behaviours in the leaf-footed bugs. In the process of this work, we discovered that seasonal changes in host plants affect the ability of the insect body to hold up to battle. We are now diving deep to understand how nutrition influences the growth and development of the insect exoskeleton more broadly. After all, a large weapon means very little if it is easily punctured or crushed during competition.
In addition to our work on male-male competition, weapons, and the insect exoskeleton, we have investigated trade-offs between the growth of weapons and testes, the plasticity and evolution in insect mouthparts, and much more. For more information, see below and our Publications page.
We use experimentation to understand the evolution of weapon size, shape, and function within species, and we use phylogenetic comparative analyses to understand cumulative changes in weapons across species. Ultimately, our interest is on the evolutionary interplay of morphology and behaviour, and weapons and physical combat provide an outstanding opportunity to understand this interaction.
We test our hypotheses in two study systems. Our long-standing study system is the superfamily of insects called the leaf-footed bugs. This group includes ~3,300 species in five extant families, and it is one of only a few animal groups that produce weapons on the hind legs. In some of these species the hind legs exhibit extreme modifications including robust spines, club-like expansions, flags, and serrations. The diversity of their hind leg shapes, their ecology, and their behaviours provide outstanding opportunities for our work. We have recently started working with the sagebrush grig, Cyphoderris strepitans, in Grand Teton National Park. Insects in this genus offer a remarkable window into sexual selection and conflict. Females choose males partly by their song, then chew on their bodies and drink their haemolymph. Males hold females in place with a specialised weapon during sperm transfer. Both sexes mate multiply, but males become weaker and less attractive after mating, losing up to 10% of their body weight in a single encounter. This extraordinary system raises fundamental questions about how conflicting reproductive interests shape behaviour and morphology.
We currently have several projects focused on how seasonally changing plant environments influence male-male competition, signalling, weapon evolution, and the evolution of sexual dimorphism. With grant funding from the National Science Foundation, our team is examining how changes in host plants affect the growth and development of animal weapons and fighting behaviours in the leaf-footed bugs. In the process of this work, we discovered that seasonal changes in host plants affect the ability of the insect body to hold up to battle. We are now diving deep to understand how nutrition influences the growth and development of the insect exoskeleton more broadly. After all, a large weapon means very little if it is easily punctured or crushed during competition.
In addition to our work on male-male competition, weapons, and the insect exoskeleton, we have investigated trade-offs between the growth of weapons and testes, the plasticity and evolution in insect mouthparts, and much more. For more information, see below and our Publications page.
Trade-offs between weapons and testes
Males in many species use weapons such as horns, antlers, and spurs to compete with other males for access to females. Larger weapons often allow males to win high-quality territories and mating opportunities. However, many of these weapons are costly to produce and maintain, competing for a limited supply of resources within the body. Through experimentation, we have discovered weapons-testes trade-offs in the leaf-footed bugs. When males do not grow a weaponized hind leg, they grow bigger testes. But, do bigger testes matter? We have found that these males also have greater sperm production and can produce more offspring with a single mating. Thus, growing weapons can come with a clear cost to other reproductive traits. Resource allocation trade-offs such as these are likely to shape the evolution of sexually selected weapons and may be partially responsible for the diversity found in these traits. We are currently expanding our approach to examine the influence of dynamic plant nutrition on trade-offs among an entire network of fitness-related traits including weapons, testes, and other traits involved in survival and reproduction.
FEATURED PAPERS
Miller CW, Joseph PN & Emberts Z (2021). Trade-offs between weapons and testes do not manifest at high social densities. Journal of Evolutionary Biology. 34: 726-735. PDF
Cavender K, Ricker T, Lyon M, Shelby E, Miller CW & Moore PJ (2021) The trade-off between investment in weapons and fertility is mediated through spermatogenesis in the leaf-footed cactus bug Narnia femorata. Ecology & Evolution. DOI: 10.1002/ece3.7686. PDF
Miller CW, Joseph PN, Kilner RM, Emberts Z (2019). A weapons–testes trade-off in males is amplified in female traits. Proceedings of the Royal Society of London (B). 286: 20190906. PDF
Joseph PN, Emberts Z, Sasson DA, & Miller CW (2018). Males that drop a sexually-selected weapon grow larger testes. Evolution. 72: 113–122. DOI: 10.1111/evo.13387. PDF
Somjee U, Miller CW, Tatarnic NJ, & Simmons LW (2018). Experimental manipulation reveals a trade-off between weapons and testes. Journal of Evolutionary Biology. 31: 57–65. DOI: 10.1111/jeb.13193. PDF
FEATURED PAPERS
Miller CW, Joseph PN & Emberts Z (2021). Trade-offs between weapons and testes do not manifest at high social densities. Journal of Evolutionary Biology. 34: 726-735. PDF
Cavender K, Ricker T, Lyon M, Shelby E, Miller CW & Moore PJ (2021) The trade-off between investment in weapons and fertility is mediated through spermatogenesis in the leaf-footed cactus bug Narnia femorata. Ecology & Evolution. DOI: 10.1002/ece3.7686. PDF
Miller CW, Joseph PN, Kilner RM, Emberts Z (2019). A weapons–testes trade-off in males is amplified in female traits. Proceedings of the Royal Society of London (B). 286: 20190906. PDF
Joseph PN, Emberts Z, Sasson DA, & Miller CW (2018). Males that drop a sexually-selected weapon grow larger testes. Evolution. 72: 113–122. DOI: 10.1111/evo.13387. PDF
Somjee U, Miller CW, Tatarnic NJ, & Simmons LW (2018). Experimental manipulation reveals a trade-off between weapons and testes. Journal of Evolutionary Biology. 31: 57–65. DOI: 10.1111/jeb.13193. PDF
Plant-insect interactions
Throughout history, animals have encountered novel foods when ranges expand, and niches shift. Today, human activities have resulted in the introduction of countless plants and insects into new contexts. When an insect encounters an edible novel plant, one of the first challenges is to figure out how to eat it. Mouthpart morphology can be critical during the process of host shifts. Developmental plasticity in mouthparts may allow animals to tolerate and eventually thrive upon new foods. Using common garden / reciprocal transplant experiments, we have found both evolved differences and pronounced developmental plasticity in the mouthparts of leaf-footed bugs in response to new plants. These changes appear to be adaptive, allowing insects to make the most of novel foods. Looking across host plants and across seasonal changes within a host plant, we have found that dietary differences can influence sexual selection and the evolvability of sexually selected traits. In the next years, we will ask how such plasticity is maintained, ready to be used. This work will incorporate developmental biology, biomechanics, behavior, and field studies of insect ecology. We also will continue to examine the consequences of feeding on seasonally dynamic host plants for the body size, shape, and behaviors of insects.
FEATURED PAPERS
Allen PE, Cui Q & Miller CW (2021). Evidence of a rapid and adaptive response of hemipteran mouthparts to a physical barrier. Journal of Evolutionary Biology 34: 653-66. PDF
Gillespie SR, Tudor MS, Moore AJ, & Miller CW (2014). Sexual selection is influenced by both developmental and adult environments. Evolution 68: 3421-3432. PDF
Miller CW & Svensson E (2014). Sexual selection in complex environments. Annual Review of Entomology 59: 427-445. PDF
Jarrett, BJM & Miller CW (2024). Host plant effects on sexual selection dynamics in phytophagous insects. Annual Review of Entomology. PDF.
Allen PE & Miller CW (2017). Novel host plant leads to the loss of sexual dimorphism in a sexually selected male weapon. Proceedings of the Royal Society of London (B). 284: 20171269. DOI: 10.1098/rspb.2017.1269. PDF
Miller CW, McDonald G, & Moore AJ (2016). The tale of the shrinking weapon: seasonal changes in nutrition affect weapon size and sexual dimorphism, but not contemporary evolution. Journal of Evolutionary Biology. 29: 2266-2275. DOI: 10.1111/jeb.12954. PDF.
FEATURED PAPERS
Allen PE, Cui Q & Miller CW (2021). Evidence of a rapid and adaptive response of hemipteran mouthparts to a physical barrier. Journal of Evolutionary Biology 34: 653-66. PDF
Gillespie SR, Tudor MS, Moore AJ, & Miller CW (2014). Sexual selection is influenced by both developmental and adult environments. Evolution 68: 3421-3432. PDF
Miller CW & Svensson E (2014). Sexual selection in complex environments. Annual Review of Entomology 59: 427-445. PDF
Jarrett, BJM & Miller CW (2024). Host plant effects on sexual selection dynamics in phytophagous insects. Annual Review of Entomology. PDF.
Allen PE & Miller CW (2017). Novel host plant leads to the loss of sexual dimorphism in a sexually selected male weapon. Proceedings of the Royal Society of London (B). 284: 20171269. DOI: 10.1098/rspb.2017.1269. PDF
Miller CW, McDonald G, & Moore AJ (2016). The tale of the shrinking weapon: seasonal changes in nutrition affect weapon size and sexual dimorphism, but not contemporary evolution. Journal of Evolutionary Biology. 29: 2266-2275. DOI: 10.1111/jeb.12954. PDF.
Dynamic host plants and the biomechanics of animal weapons
A trip to the Rocky Mountains can reveal male elk sparing with their antlers, pronghorn trying to edge out other males, and dung flies competing for mates on bison dung. In fact, any trip to the wilderness easily shows us many examples of male-male competition, or, in some cases, female-female competition over access to mates. People have been fascinated by animal weapons and their fighting behaviors for centuries. In spite of the interest, we still do not know why there is such amazing weapon diversity. Why do some species use tusks to fight over females, while others use their legs? Why do even closely-related species often have such striking differences in their weapons? And, why when a trait is this important, does it so easily break? We tackle these problems using the striking diversity of weapons in the leaf-footed bugs and their relatives (Superfamily Coreoidea). Working together with David Labonte at Imperial College in London and Walter Federle at the University of Cambridge, we are studying how plant-insect interactions influences weapon construction and diversification. Together with Michael Forthman, former postdoc in the lab, we have reconstructed the phylogeny of these insects so that we can reconstruct weapon evolution. Our research takes us to Panama, Kenya, Swaziland, South Africa, Australia, Singapore, and the southern United States. This work has been funded by multiple NSF grants, including a NSF CAREER Award.
FEATURED PAPERS
Miller CW, Kimball RT & Forthman M (2024). The evolution of multi-component weapons in the superfamily of leaf-footed bugs. Evolution 78: 635–651. Open-access link.
Greenway EV, Woodman T, Emberts Z, Chen S, Federle W & Miller CW (2024). Preprint: Adult diet strongly affects cuticle thickness and its injury resistance in the insect Narnia femorata (Hemiptera: Coreidae). bioRxiv 2024.10.22.619666; doi: https://doi.org/10.1101/2024.10.22.619666
Woodman TE, Chen S, Emberts Z, Wilner D, Federle W & Miller CW. (2021) Developmental nutrition affects the structural integrity of a sexually selected weapon. Integrative and Comparative Biology. PDF
FEATURED PAPERS
Miller CW, Kimball RT & Forthman M (2024). The evolution of multi-component weapons in the superfamily of leaf-footed bugs. Evolution 78: 635–651. Open-access link.
Greenway EV, Woodman T, Emberts Z, Chen S, Federle W & Miller CW (2024). Preprint: Adult diet strongly affects cuticle thickness and its injury resistance in the insect Narnia femorata (Hemiptera: Coreidae). bioRxiv 2024.10.22.619666; doi: https://doi.org/10.1101/2024.10.22.619666
Woodman TE, Chen S, Emberts Z, Wilner D, Federle W & Miller CW. (2021) Developmental nutrition affects the structural integrity of a sexually selected weapon. Integrative and Comparative Biology. PDF
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The Superfamily Coreoidea: There are more than 3300 species of these insects worldwide, and male hind legs are impressively diverse in shape. Males in many species (but not all) use their hind legs as weapons to wrestle over plant territories where females visit to mate, feed, and lay eggs.
Here are two male leaf-footed cactus bugs, Narnia femorata, wrestling over a territory on a nearby cactus. Males fight in intense bursts, use a variety of fighting maneuvers, and they obtain numerous injuries. Their combat behavior is a lot like mixed martial arts fighting in humans. And, below you can see the variety of shapes, sizes, and colors in this insect superfamily. |
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