Molecular early burst associated with the diversification of birds at the K–Pg boundary
This article has been Reviewed by the following groups
Listed in
- Evaluated articles (Arcadia Science)
Abstract
Complex patterns of genome and life-history evolution associated with the end-Cretaceous (K– Pg) mass extinction event limit our understanding of the early evolutionary history of crown group birds [1-9]. Here, we assess molecular heterogeneity across living birds using a technique enabling inferred sequence substitution models to transition across the history of a clade [10]. Our approach identifies distinct and contrasting regimes of molecular evolution across exons, introns, untranslated regions, and mitochondrial genomes. Up to fifteen shifts in the mode of avian molecular evolution map to rapidly diversifying clades near the Cretaceous-Palaeogene boundary, demonstrating a burst of genomic disparity early in the evolutionary history of crown birds [11-13]. Using simulation and machine learning techniques, we show that shifts in developmental mode [14] or adult body mass [4] best explain transitions in the mode of nucleotide substitution. These patterns are related, in turn, to macroevolutionary shifts in the allometric scaling relationship between basal metabolic rate and body mass [15, 16]. In agreement with theoretical predictions, this scaling relationship appears to have weakened across the end-Cretaceous transition. Overall, our study provides evidence that the Chicxulub bolide impact [17] triggered integrated patterns of evolution across avian genomes, physiology, and life history that structured the evolutionary potential of modern birds.
Article activity feed
-
-
Fifteen molecular model shifts are identified on total-clades estimated to have originated near the K–Pg boundary [43-46] (Figure 1, Supplementary Figure 1, 7a-d).
I'm curious - If you were to simulate sequences/trees under a model of mass-extinction and early burst but constant substitution rates, how often (if at all!) would Janus infer substitution rate shifts near the extinction event?
Could the extinction-driven bottleneck and heightened species turnover in the subsequent radiation amplify apparent differences in nucleotide composition even with molecular rates remaining constant? If so, could it be that alternative diversification dynamics/models impact the inference of substitution rate shifts?
-
Our analyses reveal well-supported shifts in estimated equilibrium base frequencies across exons, introns, untranslated regions (UTRs), and mitochondrial genomes. Remarkably, model shifts are mostly constrained to previously hypothesized clade originations associated with the K–Pg boundary.
Is there any chance that this pattern could, at least in part be attributed to the relative paucity of branches in the tree prior to the K-Pg boundary?
In other words, could the identification of molecular rate shifts by Janus be impacted by "sample size" differences of branches prior to and following mass extinctions as in this example?
-
we find evidence that shifts in the mode of genomic evolution were very likely concurrent with shifts in the evolutionary optima θ(t) of important avian life-history traits (Figure 2), as well as shifts in metabolic allometric slope βmass and intercept β.
Super cool - this is partly where/why the use of phylogenetic path analysis may be particularly informative - could these shifts in evolutionary optima have been associated with a shift in causal relationships among biological/life history features? Maybe it's possible to infer, at least in part, the causal mechanisms behind these shifts in metabolic allometry?
-
Overall, these patterns support the hypothesis that molecular model shifts are indicative of evolutionary shifts in life-history θ(t).
I'm not necessarily suggesting you do this, since this paper already represents an impressive effort, but I wonder whether the use of phylogenetic path analysis (https://doi.org/10.7717%2Fpeerj.4718) might be informative here?
Within each inferred molecular model shift, you could test alternative causal models depicting the relationships between rates of molecular evolution and these natural history traits, as you might anticipate that many of these covary, themselves being causally related to one another. Inference of shifts in causal relationships among natural history traits in each clade that experienced shifts in rates of molecular evolution could then provide some intuition as to why!
-
we have limited intuition about how the mode of molecular evolution may relate to life-history variation.
I'm probably sounding like a broken record now (a good thing - this is super interesting to me, and it's exciting to be nearing a place where we can address this!), but I think analysis of alternative causal models here with phylogenetic path analysis would be an awesome way towards not only generating this intuition, but also explicitly testing these hypotheses!
-
Figure 1.
How feasible would it be to infer these deviations from equilibrium base frequencies from simulated data? For instance, simulating trees/sequences under constant substitution rates (e.g. using AliSim - https://doi.org/10.1093/molbev/msac092) but under a model of mass (selective) extinction and subsequent early burst of diversification (e.g. TreeSim - https://doi.org/10.1093/sysbio/syr029)?
I ask because I wonder whether simulating under the hypothesized diversification model and constant rates of molecular evolution could provide an estimate of the false-positive rate with which Janus might infer these shifts and whether false positives tend to be concentrated around the time of the simulated mass extinction?
I realize this is probably a big ask though - the paper is already super impressive! I think this analysis could just …
Figure 1.
How feasible would it be to infer these deviations from equilibrium base frequencies from simulated data? For instance, simulating trees/sequences under constant substitution rates (e.g. using AliSim - https://doi.org/10.1093/molbev/msac092) but under a model of mass (selective) extinction and subsequent early burst of diversification (e.g. TreeSim - https://doi.org/10.1093/sysbio/syr029)?
I ask because I wonder whether simulating under the hypothesized diversification model and constant rates of molecular evolution could provide an estimate of the false-positive rate with which Janus might infer these shifts and whether false positives tend to be concentrated around the time of the simulated mass extinction?
I realize this is probably a big ask though - the paper is already super impressive! I think this analysis could just be particularly compelling evidence if in fact this concentration of events is greater than expected.
-
shifts toward weaker scaling relationships between metabolic rate and body mass (e.g., in Neoaves; Figure 3).
Would be exciting to explicitly test this!
-
The observation of a burst of molecular and quantitative trait model shifts within a ∼5 Ma interval of the K–Pg boundary (Figure 1) is likely not a coincidence
That's one possibility - though it might be worth addressing/discussing the alternative hypothesis - that the pattern of mass (and presumably non-random with respect to body size) extinction and subsequent radiation (i.e. the early burst) could lead to surviving lineages exhibiting greater disparity in rates of molecular evolution and other life history traits.
As I alluded to in my comment on figure 1, it might be worth (if feasible) explicitly assessing the probability of observing such a concentrated distribution of shifts near the time of a mass extinction event by simulating under a constant rate model of nucleotide substitution, and a mass extinction/early burst of …
The observation of a burst of molecular and quantitative trait model shifts within a ∼5 Ma interval of the K–Pg boundary (Figure 1) is likely not a coincidence
That's one possibility - though it might be worth addressing/discussing the alternative hypothesis - that the pattern of mass (and presumably non-random with respect to body size) extinction and subsequent radiation (i.e. the early burst) could lead to surviving lineages exhibiting greater disparity in rates of molecular evolution and other life history traits.
As I alluded to in my comment on figure 1, it might be worth (if feasible) explicitly assessing the probability of observing such a concentrated distribution of shifts near the time of a mass extinction event by simulating under a constant rate model of nucleotide substitution, and a mass extinction/early burst of speciation/turnover.
-
-
we have limited intuition about how the mode of molecular evolution may relate to life-history variation.
I'm probably sounding like a broken record now (a good thing - this is super interesting to me, and it's exciting to be nearing a place where we can address this!), but I think analysis of alternative causal models here with phylogenetic path analysis would be an awesome way towards not only generating this intuition, but also explicitly testing these hypotheses!
-
The observation of a burst of molecular and quantitative trait model shifts within a ∼5 Ma interval of the K–Pg boundary (Figure 1) is likely not a coincidence
That's one possibility - though it might be worth addressing/discussing the alternative hypothesis - that the pattern of mass (and presumably non-random with respect to body size) extinction and subsequent radiation (i.e. the early burst) could lead to surviving lineages exhibiting greater disparity in rates of molecular evolution and other life history traits.
As I alluded to in my comment on figure 1, it might be worth (if feasible) explicitly assessing the probability of observing such a concentrated distribution of shifts near the time of a mass extinction event by simulating under a constant rate model of nucleotide substitution, and a mass extinction/early burst of …
The observation of a burst of molecular and quantitative trait model shifts within a ∼5 Ma interval of the K–Pg boundary (Figure 1) is likely not a coincidence
That's one possibility - though it might be worth addressing/discussing the alternative hypothesis - that the pattern of mass (and presumably non-random with respect to body size) extinction and subsequent radiation (i.e. the early burst) could lead to surviving lineages exhibiting greater disparity in rates of molecular evolution and other life history traits.
As I alluded to in my comment on figure 1, it might be worth (if feasible) explicitly assessing the probability of observing such a concentrated distribution of shifts near the time of a mass extinction event by simulating under a constant rate model of nucleotide substitution, and a mass extinction/early burst of speciation/turnover.
-
shifts toward weaker scaling relationships between metabolic rate and body mass (e.g., in Neoaves; Figure 3).
Would be exciting to explicitly test this!
-
we find evidence that shifts in the mode of genomic evolution were very likely concurrent with shifts in the evolutionary optima θ(t) of important avian life-history traits (Figure 2), as well as shifts in metabolic allometric slope βmass and intercept β.
Super cool - this is partly where/why the use of phylogenetic path analysis may be particularly informative - could these shifts in evolutionary optima have been associated with a shift in causal relationships among biological/life history features? Maybe it's possible to infer, at least in part, the causal mechanisms behind these shifts in metabolic allometry?
-
Overall, these patterns support the hypothesis that molecular model shifts are indicative of evolutionary shifts in life-history θ(t).
I'm not necessarily suggesting you do this, since this paper already represents an impressive effort, but I wonder whether the use of phylogenetic path analysis (https://doi.org/10.7717%2Fpeerj.4718) might be informative here?
Within each inferred molecular model shift, you could test alternative causal models depicting the relationships between rates of molecular evolution and these natural history traits, as you might anticipate that many of these covary, themselves being causally related to one another. Inference of shifts in causal relationships among natural history traits in each clade that experienced shifts in rates of molecular evolution could then provide some intuition as to why!
-
Figure 1.
How feasible would it be to infer these deviations from equilibrium base frequencies from simulated data? For instance, simulating trees/sequences under constant substitution rates (e.g. using AliSim - https://doi.org/10.1093/molbev/msac092) but under a model of mass (selective) extinction and subsequent early burst of diversification (e.g. TreeSim - https://doi.org/10.1093/sysbio/syr029)?
I ask because I wonder whether simulating under the hypothesized diversification model and constant rates of molecular evolution could provide an estimate of the false-positive rate with which Janus might infer these shifts and whether false positives tend to be concentrated around the time of the simulated mass extinction?
I realize this is probably a big ask though - the paper is already super impressive! I think this analysis could just …
Figure 1.
How feasible would it be to infer these deviations from equilibrium base frequencies from simulated data? For instance, simulating trees/sequences under constant substitution rates (e.g. using AliSim - https://doi.org/10.1093/molbev/msac092) but under a model of mass (selective) extinction and subsequent early burst of diversification (e.g. TreeSim - https://doi.org/10.1093/sysbio/syr029)?
I ask because I wonder whether simulating under the hypothesized diversification model and constant rates of molecular evolution could provide an estimate of the false-positive rate with which Janus might infer these shifts and whether false positives tend to be concentrated around the time of the simulated mass extinction?
I realize this is probably a big ask though - the paper is already super impressive! I think this analysis could just be particularly compelling evidence if in fact this concentration of events is greater than expected.
-
Fifteen molecular model shifts are identified on total-clades estimated to have originated near the K–Pg boundary [43-46] (Figure 1, Supplementary Figure 1, 7a-d).
I'm curious - If you were to simulate sequences/trees under a model of mass-extinction and early burst but constant substitution rates, how often (if at all!) would Janus infer substitution rate shifts near the extinction event?
Could the extinction-driven bottleneck and heightened species turnover in the subsequent radiation amplify apparent differences in nucleotide composition even with molecular rates remaining constant? If so, could it be that alternative diversification dynamics/models impact the inference of substitution rate shifts?
-
Our analyses reveal well-supported shifts in estimated equilibrium base frequencies across exons, introns, untranslated regions (UTRs), and mitochondrial genomes. Remarkably, model shifts are mostly constrained to previously hypothesized clade originations associated with the K–Pg boundary.
Is there any chance that this pattern could, at least in part be attributed to the relative paucity of branches in the tree prior to the K-Pg boundary?
In other words, could the identification of molecular rate shifts by Janus be impacted by "sample size" differences of branches prior to and following mass extinctions as in this example?
-