Matthew L Holding

University of Michigan | U-M · Life Sciences Institute

Measuring local adaptation can provide insights into how coevolution occurs between predators and prey. Specifically, theory predicts that local adaptation in functionally matched traits of predators and prey will not be detected when coevolution is governed by escalating arms races, whereas it will be present when coevolution occurs through an alt...

Venom and venom resistance are molecular phenotypes widely considered to have diversified through coevolution between predators and prey. However, while evolutionary and functional studies on venom have been extensive, little is known about the molecular basis, variation, and complexity of venom resistance. We review known mechanisms of venom resis...

Within some species, squirrels respond to variable selection from venomous snake predators by showing population-level variation in resistance, while between species, some rattlesnakes possess venom that is more effective at overcoming venom resistance in different species of squirrels. A functional evaluation of resistance variation to venom withi...

Chemoreception is often crucial to the interaction between predators and their prey. Investigating the mechanisms controlling predator chemical preference gives insight into how selection molds traits directly involved in ecological interactions between species. In snakes, prey cue preferences are influenced by both direct genetic control and exper...

A fundamental component of science curricula is the understanding of scientific inquiry. Although recent trends favor using student inquiry to learn concepts through hands-on activities, it is often unclear to students where the line is drawn between the content and the process of science. This activity explicitly introduces students to the process...

Gene duplication followed by nucleotide differentiation is one of the simplest mechanisms to develop new functions for genes. However, the evolutionary processes underlying the divergence of multigene families remain controversial. We used multigene families found within the diversity of toxic proteins in centipede venom to test two hypotheses rela...

Phylogenomics allows us to uncover the historical signal of evolutionary processes through time and estimate phylogenetic networks accounting for these signals. Insight from genome-wide data further allows us to pinpoint the contributions to phylogenetic signal from hybridization, introgression, and ancestral polymorphism across the genome. Here we...

Developmental phenotypic changes can evolve under selection imposed by age- and size-related ecological differences. Many of these changes occur through programmed alterations to gene expression patterns, but the molecular mechanisms and gene-regulatory networks underlying these adaptive changes remain poorly understood. Many venomous snakes, inclu...

Background The radiation of mammals at the extinction of the dinosaurs produced a plethora of new forms—as diverse as bats, dolphins, and elephants—in only 10–20 million years. Behind the scenes, adaptation to new niches is accompanied by extensive innovation in large families of genes that allow animals to contact the environment, including chemos...

Snake venom can vary both among and within species. While some groups of New World pitvipers-such as rattlesnakes-have been well studied, very little is known about the venom of montane pitvipers (Cerrophidion) found across the Mesoamerican highlands. Compared to most well-studied rattlesnakes, which are widely distributed, the isolated montane pop...

Traits for prey acquisition form the phenotypic interface of predator–prey interactions. In venomous predators, morphological variation in venom delivery apparatus like fangs and stingers may be optimized for dispatching prey. Here, we determine how a single dimension of venom injection systems evolves in response to variation in the size, climatic...

The origin of snake venom involved duplication and recruitment of non-venom genes into venom systems. Several studies have predicted that directional positive selection has governed this process. Venom composition varies substantially across snake species and venom phenotypes are locally adapted to prey, leading to coevolutionary interactions betwe...

Understanding the molecular basis of adaptations in coevolving species requires identifying the genes that underlie reciprocally selected phenotypes, such as those involved in venom in snakes and resistance to the venom in their prey. In this regard, California ground squirrels (CGS; Otospermophilus beecheyi) are eaten by northern Pacific rattlesna...

The genomic architecture underlying the origins and maintenance of biodiversity is an increasingly accessible feature of species, due in large part to third‐generation sequencing and novel analytical toolsets. Applying these techniques to woodrats (Neotoma spp.) provides a unique opportunity to study how herbivores respond to environmental change....

Understanding the joint roles of amino acid sequences variation of proteins and differential expression during adaptive evolution is a fundamental, yet largely unrealized, goal of evolutionary biology. Here, we use phylogenetic path analysis to analyze a comprehensive venom gland transcriptome dataset spanning three genera of pitvipers to identify...

Differences in snake venom composition occur across all taxonomic levels and it has been argued that this variation represents an adaptation that has evolved to facilitate the capture and digestion of prey and evasion of predators. Bothrops atrox is a terrestrial pitviper that is distributed across the Amazon region, where it occupies different hab...

Predator-prey interactions often lead to the coevolution of adaptations associated with avoiding predation and, for predators, overcoming those defenses. Antagonistic coevolutionary relationships are often not simple interactions between a single predator and prey but rather a complex web of interactions between multiple coexisting species. Coevolu...

Venom is an integral feeding trait in many animal species. Although venom often varies ontogenetically, little is known about the proximate physiological mediators of venom variation within individuals. The glucocorticoid hormone corticosterone can alter transcription and activation of proteins, including homologues of snake venom components such a...

Local adaptation can occur when spatially separated populations are subjected to contrasting environmental conditions. Historically, understanding the genetic basis of adaptation has been difficult, but increased availability of genome‐wide markers facilitates studies of local adaptation in non‐model organisms of conservation concern. The pygmy rab...

Significance Why biological complexity evolves is a major question in the life sciences, but the specific selection pressures favoring simple or complex traits remain unclear. Using high-resolution measurements of venom complexity in North American pitvipers, we link changes in complexity to natural history via phylogenetic diversity of snake diets...

The genomic architecture underlying the origins and maintenance of biodiversity is an increasingly accessible feature of species, due in large part to third-generation sequencing and novel analytical toolsets. Woodrats of the genus Neotoma provide a unique opportunity to study how vertebrate herbivores respond to climate change, as two sister speci...

Coevolutionary theory predicts that differences in the genetic demography of interacting species can influence patterns of local adaptation by affecting the potential of local populations to respond to selection. We conducted a comparative phylogeographical study of venomous rattlesnakes and their venom-resistant ground squirrel prey across Califor...

Ontogenetic changes in venom composition have been described in Bothrops snakes, but only a few studies have attempted to identify the targeted paralogues or the molecular mechanisms involved in modifications of gene expression during ontogeny. In this study, we decoded B. jararacussu venom gland transcripts from six specimens of varying sizes and...

Ontogenetic shifts in venom occur in many snakes but establishing their nature as gradual or discrete processes required additional study. We profiled shifts in venom expression from the neonate to adult sizes of two rattlesnake species, the eastern diamondback and the timber rattlesnake. We used serial sampling and venom chromatographic profiling...

Using venom for predation often leads to the evolution of resistance in prey. Understanding individual variation in venom resistance is key to unlocking basic mechanisms by which antagonistic coevolution can sustain variation in traits under selection. For prey, the opposing challenges of predator avoidance and resource acquisition often lead to co...

Understanding how interspecific interactions mould the molecular basis of adaptations in coevolving species is a long‐sought goal of evolutionary biology. Venom in predators and venom resistance proteins in prey are coevolving molecular phenotypes, and while venoms are highly complex mixtures it is unclear if prey respond with equally complex resis...

Traits can evolve rapidly through changes in gene expression or protein-coding sequences. However, these forms of genetic variation can be correlated and changes to one can influence the other. As a result,we might expect traits lacking differential expression to preferentially evolve through changes in protein sequences or morphological adaptation...

When organisms possess chemical defenses, their predators may eventually evolve resistance to their toxins. Eastern Indigo Snakes (Drymarchon couperi; EIS) prey on pitvipers and are suspected to possess physiological resistance to their venom. In this study, we formally investigated this hypothesis using microassays that measured the ability of EIS...

Changes in gene expression can rapidly influence adaptive traits in the early stages of lineage diversification. Venom is an adaptive trait comprised of numerous toxins used for prey capture and defense. Snake venoms can vary widely between conspecific populations, but the influence of lineage diversification on such compositional differences are u...

Identifying the environmental correlates of divergence in functional traits between populations can provide insights into the evolutionary mechanisms that generate local adaptation. Here, we assess patterns of population differentiation in expressed venom proteins in Northern Pacific rattlesnakes (Crotalus oreganus) from 13 locations across Califor...

Venom-gland transcriptomics is a key tool in the study of the evolution, ecology, function, and pharmacology of animal venoms. In particular, gene-expression variation and coding sequences gained through transcriptomics provide key information for explaining functional venom variation over both ecological and evolutionary timescales. The accuracy a...

Understanding how historic habitat changes have impacted species and searching the past for clues to better understand the current plight of threatened species can help inform and improve future conservation efforts. We coupled species distribution modeling with historical imagery analysis to assess how changes in land use/land cover have influence...

Phenotypic plasticity contributes to intraspecific variation in traits of many animal species. Venom is an integral trait to the success and survival of many snake species, and potential plasticity in venom composition is important to account for in the context of basic research as well as in human medicine for treating the various symptoms of snak...

Differences in genome composition are known to influence cell division and tissue growth, yet few studies have compared tissue growth between closely related taxa that vary in ploidy and genome composition. Whether cellular mechanisms scale to a functional trait such as tissue regeneration is important for understanding the ecological interactions...

Acute stressors can be costly, often requiring alteration of normal physiological processes to mitigate their effects. Animal translocation may be a very stressful event and result in a reduced ability to maintain homeostasis. The impacts of translocation on the thermal ecology of ectothermic vertebrates, which may rely on preferred habitats for th...

Translocation, a management and conservation strategy used commonly in which animals are moved from their sites of origin to other localities, has proven controversial. We examined the physiological and behavioral impacts of repeated handling and short-distance translocation on rattlesnakes, which are often translocated from areas of human use beca...

Abstract Field endocrine studies providing new comparisons for inference into the evolutionary and ecological factors shaping organismal physiology are important, often yielding novel physiological insights. Here, we explored factors associated with the sex steroid hormone concentrations and adrenocortical response to capture stress in Hog Island b...

The hippocampus of birds and mammals plays a crucial role in spatial memory and navigation. The hippocampus exhibits plasticity in adulthood in response to diverse environmental factors associated with spatial demands placed on an animal. The medial and dorsal cortices of the telencephalon of squamate reptiles have been implicated as functional hom...

The hippocampus of birds and mammals has been shown to play a crucial role in spatial memory and navigation. The hippocampus exhibits plasticity in adulthood in response to diverse environmental factors associated with spatial demands placed on an animal. The cortical telencephalon of squamate reptiles has been implicated as a functional homologue...