Ecology drives the degree of convergence in the gene expression of extremophile fishes

Convergent evolution, where independent lineages evolve similar traits when adapting to similar habitats, is a common phenomenon and testament to the repeatability of evolutionary processes. Still, non-convergence is also common, and a major question is whether apparently idiosyncratic, lineage-specific evolutionary changes are reflective of chance events inherent to evolutionary processes, or whether they are also influenced by deterministic genetic or ecological factors. To address this question, we quantified the degree of convergence in genome-wide patterns of gene expression across lineages of livebearing fishes (family Poeciliidae) that span 40 million years of evolution and have colonized extreme environments in the form of toxic, hydrogen-sulfide-rich springs. We specifically asked whether the degree of convergence across lineage pairs was related to their phylogenetic relatedness or the ecological similarity of the habitats they inhabit. Using phylogenetic comparative analyses, we showed that the degree of convergence was highly variable across lineage pairs residing in sulfide springs. While closely related lineages did not exhibit higher degrees of convergence than distantly related ones, we uncovered a strong relationship between degree of convergence and ecological similarity. Our results indicate that variation in the degree of convergence is not merely noise associated with evolutionary contingency. Rather, cryptic environmental variation that is frequently ignored when we employ reductionist approaches can significantly contribute to adaptive evolution. This study highlights the importance of multivariate approaches that capture the complexities of both selective regimes and organismal design when assessing the roles of determinism and contingency in evolution.

Reconstruction of nitrogenase predecessors suggests origin from maturase-like enzymes

The evolution of biological nitrogen fixation, uniquely catalyzed by nitrogenase enzymes, has been one of the most consequential biogeochemical innovations over life's history. Though understanding the early evolution of nitrogen fixation has been a longstanding goal from molecular, biogeochemical, and planetary perspectives, its origins remain enigmatic. In this study, we reconstructed the evolutionary histories of nitrogenases, as well as homologous maturase proteins that participate in the assembly of the nitrogenase active-site cofactor but are not able to fix nitrogen. We combined phylogenetic and ancestral sequence inference with an analysis of predicted functionally divergent sites between nitrogenases and maturases to infer the nitrogen-fixing capabilities of their shared ancestors. Our results provide phylogenetic constraints to the emergence of nitrogen fixation and suggest that nitrogenases likely emerged from maturase-like predecessors. Though the precise functional role of such a predecessor protein remains speculative, our results highlight evolutionary contingency as a significant factor shaping the evolution of a biogeochemically essential enzyme.

Contingency and determinism in the evolution of bird song sound frequency

Sexual signals are archetypes of contingent evolution: hyper-diverse across species, often evolving fast and in unpredictable directions. It is unclear to which extent their evolutionary unpredictability weakens deterministic evolution, or takes place bounded by deterministic patterns of trait evolution. We compared the evolution of sound frequency in sexual signals (advertisement songs) and non-sexual social signals (calls) across > 500 genera of the crown songbird families. Contrary to the acoustic adaptation hypothesis, we found no evidence that forest species used lower sound frequencies in songs or calls. Consistent with contingent evolution in song, we found lower phylogenetic signal for the sound frequency of songs than calls, which suggests faster and less predictable evolution, and found unpredictable direction of evolution in lineages with longer songs, which presumably experience stronger sexual selection on song. Nonetheless, the most important deterministic pattern of sound frequency evolution—its negative association with body size—was stronger in songs than calls. This can be explained by songs being longer-range signals than most calls, and thus using sound frequencies that animals of a given size produce best at high amplitude. Results indicate that sexual selection can increase aspects of evolutionary contingency while strengthening, rather than weakening, deterministic patterns of evolution.

Exploring biological possibility through synthetic biology

This paper analyzes the notion of possibility in biology and demonstrates how synthetic biology can provide understanding on the modal dimension of biological systems. Among modal concepts, biological possibility has received surprisingly little explicit treatment in the philosophy of science. The aim of this paper is to argue for the importance of the notion of biological possibility by showing how it provides both a philosophically and biologically fruitful category as well as introducing a new practically grounded way for its assessment. More precisely, we argue that synthetic biology can provide tools to scientifically anchor reasoning about biological possibilities. Two prominent strategies for this are identified and analyzed: the design of functionally new-to-nature systems and the redesign of naturally occurring systems and their parts. These approaches allow synthetic biologists to explore systems that are not normally evolutionarily accessible and draw modal inferences that extend in scope beyond their token realizations. Subsequently, these results in synthetic biology can also be relevant for discussions on evolutionary contingency, providing new methods and insight to the study of various sources of unactualized possibilities in biology.

Contingent evolution of alternative metabolic network topologies determines whether cross-feeding evolves

Metabolic exchange is widespread in natural microbial communities and an important driver of ecosystem structure and diversity, yet it remains unclear what determines whether microbes evolve division of labor or maintain metabolic autonomy. Here we use a mechanistic model to study how metabolic strategies evolve in a constant, one resource environment, when metabolic networks are allowed to freely evolve. We find that initially identical ancestral communities of digital organisms follow different evolutionary trajectories, as some communities become dominated by a single, autonomous lineage, while others are formed by stably coexisting lineages that cross-feed on essential building blocks. Our results show how without presupposed cellular trade-offs or external drivers such as temporal niches, diverse metabolic strategies spontaneously emerge from the interplay between ecology, spatial structure, and metabolic constraints that arise during the evolution of metabolic networks. Thus, in the long term, whether microbes remain autonomous or evolve metabolic division of labour is an evolutionary contingency.