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Biology subjects

Hague, M.

Publications and source records attributed to Hague, M..

3 recordsLinked to original sources

Pervasive effects of Wolbachia on host body mass and metabolic rate

Metabolic rate is a widely variable trait that reflects organismal energy expenditure. At least half of all arthropod species carry maternally transmitted Wolbachia bacteria, but it is poorly understood how these endosymbionts affect host physiology and fitness. We tested how two central host traits, body mass and standard metabolic rate (SMR), are altered by Wolbachia for nine diverse Drosophila fly species and 13 co-occurring Wolbachia variants diverged roughly 150 million years. Interspecific trait variation was structured according to the host phylogeny, but within each host system, Wolbachia almost always altered body mass and/or SMR. Wolbachia often caused increases or decreases in body mass that, in some cases, also led to mass-dependent effects on whole-organism SMR. Other Wolbachia altered mass-adjusted SMR. These variable effects are plausibly explained by complex interactions among Wolbachia and host genomes, as documented for other traits (e.g., Wolbachia-induced cytoplasmic incompatibility). Endosymbiont effects on body mass and metabolic rate likely have cascading consequences for host biology and evolution, because these central traits are correlated with many aspects of host physiology, behavior, and life history. This also applies to hosts transinfected with Wolbachia from Drosophila to reduce the impacts of pathogens and pests on multiple continents.

evolutionary biology↗

Gene conversion facilitates the adaptive evolution of self-resistance in highly toxic newts

Reconstructing the histories of complex adaptations and identifying the evolutionary mechanisms underlying their origins are two of the primary goals of evolutionary biology. Taricha newts, which contain high concentrations of the deadly toxin tetrodotoxin (TTX) as an antipredator defense, have evolved resistance to self-intoxication, which is a complex adaptation requiring changes in six paralogs of the voltage-gated sodium channel (Nav) gene family, the physiological target of TTX. Here, we reconstruct the origins of TTX self-resistance by sequencing the entire Nav gene family in newts and related salamanders. We show that moderate TTX resistance evolved early in the salamander lineage in three of the six Nav paralogs, preceding the proposed appearance of tetrodotoxic newts by [~]100 million years. TTX-bearing newts possess additional unique substitutions across the entire Nav gene family that provide physiological TTX resistance. These substitutions coincide with signatures of positive selection and relaxed purifying selection, as well as gene conversion events, that together likely facilitated their evolution. We also identify a novel exon duplication within Nav1.4 encoding an expressed TTX-binding site. Two resistance-conferring changes within newts appear to have spread via nonallelic gene conversion: in one case, one codon was copied between paralogs, and in the second, multiple substitutions were homogenized between the duplicate exons of Nav1.4. Our results demonstrate that gene conversion can accelerate the coordinated evolution of gene families in response to a common selection pressure.

evolutionary biology↗

Genetic structure of prey populations underlies the geographic mosaic of arms race coevolution

Reciprocal adaptation is the hallmark of arms race coevolution, but the symmetry of evolutionary change between interacting species is often untested, even in the best-studied battles of natural enemies. We tested whether prey and predator exhibit symmetrical local co-adaptation in the example of a geographic mosaic of coevolution between toxic newts (Taricha granulosa) and resistant garter snakes (Thamnophis sirtalis). Prior work showing a tight correlation between levels of newt toxin and snake resistance is regarded as textbook evidence of the intense arms race between natural enemies. Here, we similarly found that toxin and resistance are functionally matched in prey and predator populations, further suggesting that mosaic variation in the armaments of both species results from the local pressures of reciprocal selection. Contrary to conventional wisdom, however, we found that local variation in newt toxin is best predicted by neutral population divergence rather than the resistance of co-occurring predators. Snake resistance, on the other hand, is clearly explained by local levels of prey toxin. Prey populations seem to structure variation in defensive toxin levels across the geographic mosaic, which in turn determines selection on predator resistance. Exaggerated armaments suggest that coevolution occurs in certain hotspots, but our results imply that neutral processes like gene flow--rather than reciprocal adaptation--structure the greatest source of variation across the landscape. This pattern supports the predicted role of \"trait remixing\" in the geographic mosaic of coevolution, the process by which non-adaptive forces dictate spatial variation in the interactions among species.\n\nSIGNIFICANCE STATEMENTWhen the weapons of natural enemies like prey toxins and predator resistance are matched across the geographic landscape, they are usually presumed to result from arms race coevolution. In the textbook example of an arms race, matched levels of newt toxin and garter snake resistance have long been regarded as evidence of such local co-adaptation. To the contrary, we found that local variation in newt toxicity is best explained by the neutral geographic structure of newt populations. This spatial variation of prey in turn dictates local selection on garter snakes, structuring the geographic pattern of predator resistance. These results demonstrate how landscape patterns of phenotypic variation are determined by a mixture of natural selection, historical biogeography, and gene flow that comprise the geographic mosaic of coevolution.

evolutionary biology↗