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1.  Parallel Evolution of Tetrodotoxin Resistance in Three Voltage-Gated Sodium Channel Genes in the Garter Snake Thamnophis sirtalis 
Molecular Biology and Evolution  2014;31(11):2836-2846.
Members of a gene family expressed in a single species often experience common selection pressures. Consequently, the molecular basis of complex adaptations may be expected to involve parallel evolutionary changes in multiple paralogs. Here, we use bacterial artificial chromosome library scans to investigate the evolution of the voltage-gated sodium channel (Nav) family in the garter snake Thamnophis sirtalis, a predator of highly toxic Taricha newts. Newts possess tetrodotoxin (TTX), which blocks Nav’s, arresting action potentials in nerves and muscle. Some Thamnophis populations have evolved resistance to extremely high levels of TTX. Previous work has identified amino acid sites in the skeletal muscle sodium channel Nav1.4 that confer resistance to TTX and vary across populations. We identify parallel evolution of TTX resistance in two additional Nav paralogs, Nav1.6 and 1.7, which are known to be expressed in the peripheral nervous system and should thus be exposed to ingested TTX. Each paralog contains at least one TTX-resistant substitution identical to a substitution previously identified in Nav1.4. These sites are fixed across populations, suggesting that the resistant peripheral nerves antedate resistant muscle. In contrast, three sodium channels expressed solely in the central nervous system (Nav1.1–1.3) showed no evidence of TTX resistance, consistent with protection from toxins by the blood–brain barrier. We also report the exon–intron structure of six Nav paralogs, the first such analysis for snake genes. Our results demonstrate that the molecular basis of adaptation may be both repeatable across members of a gene family and predictable based on functional considerations.
doi:10.1093/molbev/msu237
PMCID: PMC4209135  PMID: 25135948
adaptation; coevolution; gene families; molecular evolution; predator–prey interactions; toxins
2.  Interspecific Aggression and Habitat Partitioning in Garter Snakes 
PLoS ONE  2014;9(1):e86208.
Defense of a limited resource, such as space or food, has recently been discovered in snakes and has been widely documented in lizards. Garter snakes (Thamnophis spp.) are historically considered generalist predators such that food is not a limiting resource. However, in this study we show that the common garter snake (Thamnophis sirtalis) and the aquatic garter snake (Thamnophis atratus) show a strong preference for amphibians as their primary food source at the Santa Lucia Preserve (SLP), Monterey County, California. This food preference forces these snake species at SLP to exploit aquatic habitats. Our principle goal was to investigate the aggressive behavior of T. sirtalis and the potential that this aggression displaces T. atratus from its preferred habitat. We found that when individuals from either species are alone, a 100% preference for aquatic or near aquatic habitat is observed. In contrast, when these species are together, T. sirtalis occupy the aquatic habitat and T. atratus occupy an area far removed from water. Thamnophis sirtalis often physically force T. atratus from the aquatic habitat through repeated biting and other displays of aggression.
doi:10.1371/journal.pone.0086208
PMCID: PMC3899215  PMID: 24465962
3.  Fine-scale selection by ovipositing females increases egg survival 
Ecology and Evolution  2012;2(11):2763-2774.
One of the most important defenses for the eggs of ovipositing female organisms is to avoid being laid in the same habitat as their predators. However, for most organisms, completely avoiding an offspring's predators is not possible. One mechanism that has been largely overlooked is for females to partition an oviposition site into microhabitats that differ in quality for offspring survival. We conducted a series of experiments to examine whether female newts avoid microhabitats utilized by their offspring's primary predator, caddisfly larvae. Female newts avoided laying eggs near predatory caddisflies and shifted egg laying upward in the water column when provided with a vertical dimension. Caddisflies were attracted to chemical stimuli from female newts and their eggs, yet primarily used benthic areas in experimental chambers. Finally, results from a field experiment indicate that the behavioral strategy employed by female newts increases offspring survival. This subset of non-genetic maternal effects, micro-oviposition avoidance, is likely an important yet underexplored mechanism by which females increase offspring survival.
doi:10.1002/ece3.389
PMCID: PMC3501628  PMID: 23170211
Choice; habitat selection; oviposition; Taricha granulosa; tetrodotoxin
4.  Genetic architecture of a feeding adaptation: garter snake (Thamnophis) resistance to tetrodotoxin bearing prey 
Detailing the genetic basis of adaptive variation in natural populations is a first step towards understanding the process of adaptive evolution, yet few ecologically relevant traits have been characterized at the genetic level in wild populations. Traits that mediate coevolutionary interactions between species are ideal for studying adaptation because of the intensity of selection and the well-characterized ecological context. We have previously described the ecological context, evolutionary history and partial genetic basis of tetrodotoxin (TTX) resistance in garter snakes (Thamnophis). Derived mutations in a voltage-gated sodium channel gene (Nav1.4) in three garter snake species are associated with resistance to TTX, the lethal neurotoxin found in their newt prey (Taricha). Here we evaluate the contribution of Nav1.4 alleles to TTX resistance in two of those species from central coastal California. We measured the phenotypes (TTX resistance) and genotypes (Nav1.4 and microsatellites) in a local sample of Thamnophis atratus and Thamnophis sirtalis. Allelic variation in Nav1.4 explains 23 per cent of the variation in TTX resistance in T. atratus while variation in a haphazard sample of the genome (neutral microsatellite markers) shows no association with the phenotype. Similarly, allelic variation in Nav1.4 correlates almost perfectly with TTX resistance in T. sirtalis, but neutral variation does not. These strong correlations suggest that Nav1.4 is a major effect locus. The simple genetic architecture of TTX resistance in garter snakes may significantly impact the dynamics of phenotypic coevolution. Fixation of a few alleles of major effect in some garter snake populations may have led to the evolution of extreme phenotypes and an ‘escape’ from the arms race with newts.
doi:10.1098/rspb.2010.0748
PMCID: PMC2981930  PMID: 20522513
adaptation; gene of major effect; coevolution; Thamnophis; tetrodotoxin; sodium channel
5.  Phenotypic Mismatches Reveal Escape from Arms-Race Coevolution 
PLoS Biology  2008;6(3):e60.
Because coevolution takes place across a broad scale of time and space, it is virtually impossible to understand its dynamics and trajectories by studying a single pair of interacting populations at one time. Comparing populations across a range of an interaction, especially for long-lived species, can provide insight into these features of coevolution by sampling across a diverse set of conditions and histories. We used measures of prey traits (tetrodotoxin toxicity in newts) and predator traits (tetrodotoxin resistance of snakes) to assess the degree of phenotypic mismatch across the range of their coevolutionary interaction. Geographic patterns of phenotypic exaggeration were similar in prey and predators, with most phenotypically elevated localities occurring along the central Oregon coast and central California. Contrary to expectations, however, these areas of elevated traits did not coincide with the most intense coevolutionary selection. Measures of functional trait mismatch revealed that over one-third of sampled localities were so mismatched that reciprocal selection could not occur given current trait distributions. Estimates of current locality-specific interaction selection gradients confirmed this interpretation. In every case of mismatch, predators were “ahead” of prey in the arms race; the converse escape of prey was never observed. The emergent pattern suggests a dynamic in which interacting species experience reciprocal selection that drives arms-race escalation of both prey and predator phenotypes at a subset of localities across the interaction. This coadaptation proceeds until the evolution of extreme phenotypes by predators, through genes of large effect, allows snakes to, at least temporarily, escape the arms race.
Author Summary
Arms races between natural enemies can lead to the rapid evolution of extreme traits, high degrees of specialization, and the formation of new species. They also serve as the ecological model for the evolution of drug resistance by diseases and for host–pathogen interactions in general. Revealing who wins these arms races and how they do so is critical to our understanding of these processes. Capitalizing on the geographic mosaic of species interactions, we examined the dynamics of the arms race between snakes and their toxic newt prey. Garter snakes in some populations have evolved dramatic resistance to the tetrodotoxin defense of the their local prey. By evaluating the pattern of mismatches between toxicity and resistance, we discovered that predators sometimes escape the arms race through the evolution of extreme resistance, but that prey never come out ahead. The reason for this one-sided outcome appears to depend on the molecular genetic basis of resistance in snakes, wherein changes to a single amino acid residue can confer huge differences in resistance.
Who wins in the arms race between predators and prey? In the interaction between snakes and toxic newts, predators sometimes escape the arms race through the evolution of extreme resistance, but prey never come out ahead.
doi:10.1371/journal.pbio.0060060
PMCID: PMC2265764  PMID: 18336073
6.  Confirmation and Distribution of Tetrodotoxin for the First Time in Terrestrial Invertebrates: Two Terrestrial Flatworm Species (Bipalium adventitium and Bipalium kewense) 
PLoS ONE  2014;9(6):e100718.
The potent neurotoxin tetrodotoxin (TTX) is known from a diverse array of taxa, but is unknown in terrestrial invertebrates. Tetrodotoxin is a low molecular weight compound that acts by blocking voltage-gated sodium channels, inducing paralysis. However, the origins and ecological functions of TTX in most taxa remain mysterious. Here, we show that TTX is present in two species of terrestrial flatworm (Bipalium adventitium and Bipalium kewense) using a competitive inhibition enzymatic immunoassay to quantify the toxin and high phase liquid chromatography to confirm the presence. We also investigated the distribution of TTX throughout the bodies of the flatworms and provide evidence suggesting that TTX is used during predation to subdue large prey items. We also show that the egg capsules of B. adventitium have TTX, indicating a further role in defense. These data suggest a potential route for TTX bioaccumulation in terrestrial systems.
doi:10.1371/journal.pone.0100718
PMCID: PMC4070999  PMID: 24963791
7.  Quantitative genetic versions of Hamilton's rule with empirical applications 
Hamilton's theory of inclusive fitness revolutionized our understanding of the evolution of social interactions. Surprisingly, an incorporation of Hamilton's perspective into the quantitative genetic theory of phenotypic evolution has been slow, despite the popularity of quantitative genetics in evolutionary studies. Here, we discuss several versions of Hamilton's rule for social evolution from a quantitative genetic perspective, emphasizing its utility in empirical applications. Although evolutionary quantitative genetics offers methods to measure each of the critical parameters of Hamilton's rule, empirical work has lagged behind theory. In particular, we lack studies of selection on altruistic traits in the wild. Fitness costs and benefits of altruism can be estimated using a simple extension of phenotypic selection analysis that incorporates the traits of social interactants. We also discuss the importance of considering the genetic influence of the social environment, or indirect genetic effects (IGEs), in the context of Hamilton's rule. Research in social evolution has generated an extensive body of empirical work focusing—with good reason—almost solely on relatedness. We argue that quantifying the roles of social and non-social components of selection and IGEs, in addition to relatedness, is now timely and should provide unique additional insights into social evolution.
doi:10.1098/rstb.2013.0358
PMCID: PMC3982660  PMID: 24686930
inclusive fitness theory; indirect genetic effects; kin selection; quantitative genetics; relatedness; social selection
8.  Developmental and Evolutionary History Affect Survival in Stressful Environments 
PLoS ONE  2014;9(4):e95174.
The world is increasingly impacted by a variety of stressors that have the potential to differentially influence life history stages of organisms. Organisms have evolved to cope with some stressors, while with others they have little capacity. It is thus important to understand the effects of both developmental and evolutionary history on survival in stressful environments. We present evidence of the effects of both developmental and evolutionary history on survival of a freshwater vertebrate, the rough-skinned newt (Taricha granulosa) in an osmotically stressful environment. We compared the survival of larvae in either NaCl or MgCl2 that were exposed to salinity either as larvae only or as embryos as well. Embryonic exposure to salinity led to greater mortality of newt larvae than larval exposure alone, and this reduced survival probability was strongly linked to the carry-over effect of stunted embryonic growth in salts. Larval survival was also dependent on the type of salt (NaCl or MgCl2) the larvae were exposed to, and was lowest in MgCl2, a widely-used chemical deicer that, unlike NaCl, amphibian larvae do not have an evolutionary history of regulating at high levels. Both developmental and evolutionary history are critical factors in determining survival in this stressful environment, a pattern that may have widespread implications for the survival of animals increasingly impacted by substances with which they have little evolutionary history.
doi:10.1371/journal.pone.0095174
PMCID: PMC3991610  PMID: 24748021
9.  Surprisingly little population genetic structure in a fungus-associated beetle despite its exploitation of multiple hosts 
Ecology and Evolution  2013;3(6):1484-1494.
In heterogeneous environments, landscape features directly affect the structure of genetic variation among populations by functioning as barriers to gene flow. Resource-associated population genetic structure, in which populations that use different resources (e.g., host plants) are genetically distinct, is a well-studied example of how environmental heterogeneity structures populations. However, the pattern that emerges in a given landscape should depend on its particular combination of resources. If resources constitute barriers to gene flow, population differentiation should be lowest in homogeneous landscapes, and highest where resources exist in equal proportions. In this study, we tested whether host community diversity affects population genetic structure in a beetle (Bolitotherus cornutus) that exploits three sympatric host fungi. We collected B. cornutus from plots containing the three host fungi in different proportions and quantified population genetic structure in each plot using a panel of microsatellite loci. We found no relationship between host community diversity and population differentiation in this species; however, we also found no evidence of resource-associated differentiation, suggesting that host fungi are not substantial barriers to gene flow. Moreover, we detected no genetic differentiation among B. cornutus populations separated by several kilometers, even though a previous study demonstrated moderate genetic structure on the scale of a few hundred meters. Although we found no effect of community diversity on population genetic structure in this study, the role of host communities in the structuring of genetic variation in heterogeneous landscapes should be further explored in a species that exhibits resource-associated population genetic structure.
doi:10.1002/ece3.560
PMCID: PMC3686185  PMID: 23789061
Bolitotherus cornutus; community diversity; environmental heterogeneity; resource-associated population structure
10.  Potential for local adaptation in response to an anthropogenic agent of selection: effects of road deicing salts on amphibian embryonic survival and development 
Evolutionary Applications  2012;6(2):384-392.
The application of millions of tons of road deicing salts every winter in North America presents significant survival challenges to amphibians inhabiting roadside habitats. While much is known of the effects of NaCl on anuran tadpoles, less is known of effects on amphibian eggs, or any caudate life stage. In addition, little is known of the effects of MgCl2, which is now the 2nd most commonly used road deicer. Most studies have considered amphibians to be helpless victims of deicing salts, and ignore the possibility of the evolution of local adaptation to this stressor. We attempt to address these knowledge gaps and explore this evolutionary potential by examining the effects of NaCl and MgCl2 on the survival and development of eggs from different female rough-skinned newts (Taricha granulosa) from the same population. We demonstrate that both salts, at environmentally relevant concentrations, severely affect the embryonic survival and development of this amphibian, but that the effects of the salt are dependent on the identity of the mother. This female × treatment interaction results in substantial variation in tolerance to road deicing salts among newt families, providing the raw material necessary for natural selection and the evolution of local adaptation in this amphibian.
doi:10.1111/eva.12016
PMCID: PMC3586626  PMID: 23467723
amphibian; egg; local adaptation; magnesium chloride; natural selection; road deicing salt; Taricha granulosa; variation
11.  Do All Portable Cases Constructed by Caddisfly Larvae Function in Defense? 
The portable cases constructed by caddisfly larvae have been assumed to act as a mechanical defense against predatory attacks. However, previous studies have compared the survival of caddisflies with different cases, thereby precluding an analysis of the survival benefits of “weaker” case materials. The level of protection offered by caddisfly cases constructed with rock, stick, or leaf material, as well as a no-case control, was investigated against predatory dragonfly nymphs (Anax junius Drury (Anisoptera: Aeshnidae)). A valid supposition is that the cases made of stronger material are more effective at deterring predators. Yet, observations revealed that there was no difference in survival between the case types. All caddisflies with a case experienced high survival in comparison to caddisflies removed from their case. In addition, larvae with stick-cases experienced fewer attacks and captures by dragonflies. These results showed that the presence of a case, regardless of the material used in its construction, offers survival benefits when faced with predatory dragonfly nymphs.
doi:10.1673/031.013.0501
PMCID: PMC3735051  PMID: 23879246
dragonfly; Odonata; survival; Trichoptera
12.  Morphological Correlates of a Combat Performance Trait in the Forked Fungus Beetle, Bolitotherus cornutus 
PLoS ONE  2012;7(8):e42738.
Combat traits are thought to have arisen due to intense male-male competition for access to females. While large and elaborate weapons used in attacking other males have often been the focus of sexual selection studies, defensive traits (both morphological and performance) have received less attention. However, if defensive traits help males restrict access to females, their role in the process of sexual selection could also be important. Here we examine the morphological correlates of grip strength, a defensive combat trait involved in mate guarding, in the tenebrionid beetle Bolitotherus cornutus. We found that grip strength was repeatable and differed between the sexes. However, these differences in performance were largely explained by body size and a non-additive interaction between size and leg length that differed between males and females. Our results suggest that leg size and body size interact as part of an integrated suite of defensive combat traits.
doi:10.1371/journal.pone.0042738
PMCID: PMC3419742  PMID: 22916153
13.  Interfamily variation in amphibian early life-history traits: raw material for natural selection? 
Ecology and Evolution  2012;2(7):1637-1643.
The embryonic development and time to hatching of eggs can be highly adaptive in some species, and thus under selective pressure. In this study, we examined the underlying interfamily variation in hatching timing and embryonic development in a population of an oviparous amphibian, the rough-skinned newt (Taricha granulosa). We found significant, high variability in degree of embryonic development and hatching timing among eggs from different females. Patterns of variation were present regardless of temperature. We also could not explain the differences among families by morphological traits of the females or their eggs. This study suggests that the variation necessary for natural selection to act upon is present in the early life history of this amphibian.
doi:10.1002/ece3.287
PMCID: PMC3434928  PMID: 22957168
Amphibian; egg; embryonic development; hatching; Salamandridae; Taricha granulosa; variation
15.  A proposal to sequence the genome of a garter snake (Thamnophis sirtalis) 
Standards in Genomic Sciences  2011;4(2):257-270.
Here we develop an argument in support of sequencing a garter snake (Thamnophis sirtalis) genome, and outline a plan to accomplish this. This snake is a common, widespread, nonvenomous North American species that has served as a model for diverse studies in evolutionary biology, physiology, genomics, behavior and coevolution. The anole lizard is currently the only genome sequence available for a non-avian reptile. Thus, the garter snake at this time would be the first available snake genome sequence and as such would provide much needed comparative representation of non-avian reptilian genomes, and would also allow critical new insights for vertebrate comparative genomic studies. We outline the major areas of discovery that the availability of the garter snake genome would enable, and describe a plan for whole-genome sequencing.
doi:10.4056/sigs.1664145
PMCID: PMC3111982  PMID: 21677863
16.  Maternal food provisioning in relation to condition-dependent offspring odours in burrower bugs (Sehirus cinctus) 
The sensory modalities used for communication among family members have at least partly evolved within an organism's pre-existing sensory context. Given the well-known general importance of chemical communication in insects, we hypothesized in sub-social insects with parental care that chemical signals emitted by larvae to influence parental care (i.e. solicitation pheromones) would have evolved. To test this hypothesis, we performed an experiment in the burrower bug Sehirus cinctus (Hemiptera: Cydnidae) where nymphs were hand-reared under high- or low-food conditions. These hand-reared clutches were used as a source of volatiles. The volatiles were collected for chemical analysis and delivered to caring mothers to quantify their behavioural response. As predicted, mothers exposed to volatiles from nymphs in poor condition provisioned significantly more food than those exposed to air (controls) or volatiles from high-condition nymphs. Chemical analysis revealed that nymphs emitted a blend of eight compounds of which α-pinene and camphene showed the strongest relationship with food treatment. Exposure to pure synthetic α-pinene and camphene did not affect maternal provisioning, however, suggesting that the functional significance of α-pinene and/or camphene may occur in a blend with other compounds. This study shows a clear effect of condition-dependent offspring odours on maternal food provisioning and identifies, for the first time, candidate compounds for a potential chemical offspring begging signal.
doi:10.1098/rspb.2006.3475
PMCID: PMC1560311  PMID: 16777747
parental care; begging; family conflicts; chemical communication; Sehirus cinctus
17.  Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transmission. 
The past 30 years of immunological research have revealed much about the proximate mechanisms of maternal antibody transmission and utilization, but have not adequately addressed how these issues are related to evolutionary and ecological theory. Much remains to be learned about individual differences within a species in maternal antibody transmission as well as differences among species in transmission or utilization of antibodies. Similarly, maternal-effects theory has generally neglected the mechanisms by which mothers influence offspring phenotype. Although the environmental cues that generate maternal effects and the consequent effects for offspring phenotype are often well characterized, the intermediary physiological and developmental steps through which the maternal effect is transmitted are generally unknown. Integration of the proximate mechanisms of maternal antibody transmission with evolutionary theory on maternal effects affords an important opportunity to unite mechanism and process by focusing on the links between genetics, environment and physiology, with the ultimate goal of explaining differences among individuals and species in the transfer of immune function from one generation to the next.
doi:10.1098/rspb.2003.2485
PMCID: PMC1691520  PMID: 14667346

Results 1-17 (17)