Gradual and Discrete Ontogenetic Shifts in Rattlesnake Venom Composition and Assessment of Hormonal and Ecological Correlates.

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 to test if ontogenetic change occurs gradually or discretely. We found evidence for gradual shifts in overall venom composition in six of eight snakes, which sometimes spanned more than two years. Most chromatographic peaks shift gradually, but one quarter shift in a discrete fashion. Analysis of published diet data showed gradual shifts in overall diet composition across the range of body sizes attained by our eight study animals, while the shifts in abundance of different prey classes varied in form from gradual to discrete. Testosterone concentrations were correlated with the change in venom protein composition, but the relationship is not strong enough to suggest causation. Venom research employing simple juvenile versus adult size thresholds may be failing to account for continuous variation in venom composition lifespan. Our results imply that venom shifts represent adaptive matches to dietary shifts and highlight venom for studies of alternative gene regulatory mechanisms.

No Cost of Complexity in Bacteriophages Adapting to a Complex Environment.

A long-standing prediction in evolutionary biology is that organisms experience a so-called "cost of complexity" manifested as a decreasing rate of adaptation in populations as organisms or selective environments become increasingly complex. This theory assumes the ubiquity of antagonistic pleiotropy, or trade-offs in fitness, for mutations affecting multiple traits or phenotypes. A particular manifestation of antagonism thought to be at play in adaptive dynamics involves the relationship between viral growth rate and capsid stability, an interaction that may impede the adaptation of viral pathogens to novel hosts and environments. Here, we present a comparison of the genetics of adaptation for populations of bacteriophages undergoing complete adaptive walks under both simple and complex selective conditions, with complexity being determined by the number of traits under directional selection. We found no evidence for a long-term cost of complexity in viruses experiencing complex selection, with on average at least as great a rate of adaptation under more complex conditions, and rampant evidence for synergistic, rather than antagonistic, pleiotropy. The lack of evident trade-offs between multiple phenotypes implies that emerging pathogens may be able to improve their growth in many different hosts or environments simultaneously, and to do so at a faster rate than previously anticipated.

Synergistic Pleiotropy Overrides the Costs of Complexity in Viral Adaptation.

Adaptive evolution progresses as a series of steps toward a multidimensional phenotypic optimum, and organismal or environmental complexity determines the number of phenotypic dimensions, or traits, under selection. Populations evolving in complex environments may experience costs of complexity such that improvement in one or more traits is impeded by selection on others. We compared the fitness effects of the first fixed mutations for populations of single-stranded DNA bacteriophage evolving under simple selection for growth rate to those of populations evolving under more complex selection for growth rate as well as capsid stability. We detected a cost of complexity manifested as a smaller growth rate improvement for mutations fixed under complex conditions. We found that, despite imposing a cost for growth rate improvement, strong complex selection resulted in the greatest overall fitness improvement, even for single mutations. Under weaker secondary selective pressures, tradeoffs between growth rate and stability were pervasive, but strong selection on the secondary trait resulted largely in mutations beneficial to both traits. Strength of selection therefore determined the nature of pleiotropy governing observed trait evolution, and strong positive selection forced populations to find mutations that improved multiple traits, thereby overriding costs incurred as a result of a more complex selective environment. The costs of complexity, however, remained substantial when considering the effects on a single trait in the context of selection on multiple traits.