Dataset Information

The million-year wait for macroevolutionary bursts.

ABSTRACT: We lack a comprehensive understanding of evolutionary pattern and process because short-term and long-term data have rarely been combined into a single analytical framework. Here we test alternative models of phenotypic evolution using a dataset of unprecedented size and temporal span (over 8,000 data points). The data are body-size measurements taken from historical studies, the fossil record, and among-species comparative data representing mammals, squamates, and birds. By analyzing this large dataset, we identify stochastic models that can explain evolutionary patterns on both short and long timescales and reveal a remarkably consistent pattern in the timing of divergence across taxonomic groups. Even though rapid, short-term evolution often occurs in intervals shorter than 1 Myr, the changes are constrained and do not accumulate over time. Over longer intervals (1-360 Myr), this pattern of bounded evolution yields to a pattern of increasing divergence with time. The best-fitting model to explain this pattern is a model that combines rare but substantial bursts of phenotypic change with bounded fluctuations on shorter timescales. We suggest that these rare bursts reflect permanent changes in adaptive zones, whereas the short-term fluctuations represent local variations in niche optima due to restricted environmental variation within a stable adaptive zone.

SUBMITTER: Uyeda JC

PROVIDER: S-EPMC3179053 | biostudies-literature | 2011 Sep

REPOSITORIES: biostudies-literature

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The million-year wait for macroevolutionary bursts.

Uyeda Josef C JC Hansen Thomas F TF Arnold Stevan J SJ Pienaar Jason J

Proceedings of the National Academy of Sciences of the United States of America 20110823 38

We lack a comprehensive understanding of evolutionary pattern and process because short-term and long-term data have rarely been combined into a single analytical framework. Here we test alternative models of phenotypic evolution using a dataset of unprecedented size and temporal span (over 8,000 data points). The data are body-size measurements taken from historical studies, the fossil record, and among-species comparative data representing mammals, squamates, and birds. By analyzing this large ...[more]

PMID: 21873251

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Project description:BACKGROUND:Bird plumage exhibits a diversity of colors that serve functional roles ranging from signaling to camouflage and thermoregulation. However, birds must maintain a balance between evolving colorful signals to attract mates, minimizing conspicuousness to predators, and optimizing adaptation to climate conditions. Examining plumage color macroevolution provides a framework for understanding this dynamic interplay over phylogenetic scales. Plumage evolution due to a single overarching process, such as selection, may generate the same macroevolutionary pattern of color variation across all body regions. In contrast, independent processes may partition plumage and produce region-specific patterns. To test these alternative scenarios, we collected color data from museum specimens of an ornate clade of birds, the Australasian lorikeets, using visible-light and UV-light photography, and comparative methods. We predicted that the diversification of homologous feather regions, i.e., patches, known to be involved in sexual signaling (e.g., face) would be less constrained than patches on the back and wings, where new color states may come at the cost of crypsis. Because environmental adaptation may drive evolution towards or away from color states, we tested whether climate more strongly covaried with plumage regions under greater or weaker macroevolutionary constraint. RESULTS:We found that alternative macroevolutionary models and varying rates best describe color evolution, a pattern consistent with our prediction that different plumage regions evolved in response to independent processes. Modeling plumage regions independently, in functional groups, and all together showed that patches with similar macroevolutionary models clustered together into distinct regions (e.g., head, wing, belly), which suggests that plumage does not evolve as a single trait in this group. Wing patches, which were conserved on a macroevolutionary scale, covaried with climate more strongly than plumage regions (e.g., head), which diversified in a burst. CONCLUSIONS:Overall, our results support the hypothesis that the extraordinary color diversity in the lorikeets was generated by a mosaic of evolutionary processes acting on plumage region subsets. Partitioning of plumage regions in different parts of the body provides a mechanism that allows birds to evolve bright colors for signaling and remain hidden from predators or adapt to local climatic conditions.

Project description:Beneath the seafloor, microbial life subsists in isolation from the surface world under persistent energy limitation. The nature and extent of genomic evolution in subseafloor microbes have been unknown. Here, we show that the genomes of Thalassospira bacterial populations cultured from million-year-old subseafloor sediments evolve in clonal populations by point mutation, with a relatively low rate of homologous recombination and elevated numbers of pseudogenes. Ratios of nonsynonymous to synonymous substitutions correlate with the accumulation of pseudogenes, consistent with a role for genetic drift in the subseafloor strains but not in type strains of Thalassospira isolated from the surface world. Consistent with this, pangenome analysis reveals that the subseafloor bacterial genomes have a significantly lower number of singleton genes than the type strains, indicating a reduction in recent gene acquisitions. Numerous insertion-deletion events and pseudogenes were present in a flagellar operon of the subseafloor bacteria, indicating that motility is nonessential in these million-year-old subseafloor sediments. This genomic evolution in subseafloor clonal populations coincided with a phenotypic difference: all subseafloor isolates have a lower rate of growth under laboratory conditions than the Thalassospira xiamenensis type strain. Our findings demonstrate that the long-term physical isolation of Thalassospira, in the absence of recombination, has resulted in clonal populations whereby reduced access to novel genetic material from neighbors has resulted in the fixation of new mutations that accumulate in genomes over millions of years. IMPORTANCE The nature and extent of genomic evolution in subseafloor microbial populations subsisting for millions of years below the seafloor are unknown. Subseafloor populations have ultralow metabolic rates that are hypothesized to restrict reproduction and, consequently, the spread of new traits. Our findings demonstrate that genomes of cultivated bacterial strains from the genus Thalassospira isolated from million-year-old abyssal sediment exhibit greatly reduced levels of homologous recombination, elevated numbers of pseudogenes, and genome-wide evidence of relaxed purifying selection. These substitutions and pseudogenes are fixed into the population, suggesting that the genome evolution of these bacteria has been dominated by genetic drift. Thus, reduced recombination, stemming from long-term physical isolation, resulted in small clonal populations of Thalassospira that have accumulated mutations in their genomes over millions of years.

Dataset Information

The million-year wait for macroevolutionary bursts.

Publications

The million-year wait for macroevolutionary bursts.

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