The tree balance signature of mass extinction is erased by continued evolution in clades of constrained size with trait-dependent speciation

Abstract

The kind and duration of phylogenetic topological "signatures" left in the wake of macroevolutionary events remain poorly understood. To this end, we examined a broad range of simulated phylogenies generated using trait-biased, heritable speciation probabilities and mass extinction that could be either random or selective on trait value, but also using background extinction and diversity-dependence to constrain clade sizes. In keeping with prior results, random mass extinction increased imbalance of clades that recovered to pre-extinction size, but was a relatively weak effect. Mass extinction that was selective on trait values tended to produce clades of similar or greater balance compared to random extinction or controls. Allowing evolution to continue past the point of clade-size recovery resulted in erosion and eventual erasure of this signal, with all treatments converging on similar values of imbalance, except for very intense extinction regimes targeted at taxa with high speciation rates. Return to a more balanced state with extended post-extinction evolution was also associated with loss of the previous phylogenetic root in most treatments. These results further demonstrate that while a mass extinction event can produce a recognizable phylogenetic signal, its effects become increasingly obscured the further an evolving clade gets from that event, with any sharp imbalance due to unrelated evolutionary factors.

Fig 1. Change in tree balance at select time points after mass extinction episode in communities of avida digital organisms.

Data previously unpublished from Yedid et al. (2012). Mass extinction treatments were applied randomly and instantaneously (pulse) or by massive environmental change over a period of time (press), at strong and weak intensities. The y-axis is Aldous’ β [β_A, 16], a measure of tree balance applicable to non-dichotomous trees; a Yule expectation is around zero, while more negative values indicate trees more imbalanced than this expectation. Data points are averages of 100 replicates ± 2 standard errors. Solid traces are maximum likelihood estimates of β_A, dashed traces are 95% confidence intervals around the calculated β_A estimates. β_A values (with confidence intervals) were determined using a customized version of the maxlik.betasplit function in the R package apTreeshape (courtesy M. Blum).

Fig 2. Effect of mass extinction and recovery beyond clade-size recovery using Blum et al.’s [21] Yule-standardized version of Colless’ [15] index of imbalance.

CSR = clade-size recovery; CSR/END 1QTR, MID, 3QTR = CSR/end simulation first-quarter, midpoint and three-quarter points; END SIM = end-simulation. RAND = random extinction; SOD = selective-on-diversifiers; SOR = selective-on-relicts. 0.5, 0.75, and 0.9 refer to extinction intensity. Short-dashed lines above and below the zero line indicate boundaries of inner Yule zone; long-dashed lines indicate outer Yule zone boundaries. All data points are averages of 100 replicates ± 2 standard errors. See Methods for statistical analysis and special statistical treatment regarding Control.

Fig 3. Exemplar phylogenetic trees showing change in balance and trait/rate values over time.

Branch lengths are scaled in MeSA absolute time. These trees correspond to the histograms of trait variance shown in S5 Fig. Tips are coloured according to trait value ranges shown in colour scale at bottom.

1. a)

   t = 165, trait variance approximately 1, increasing

2. b)

   t = 320, trait variance at half-maximum, increasing

3. c)

   t = 400, maximum variance

4. d)

   t = 420, half-maximum, descending

5. e)

   t = 520, variance < 1 but still strong imbalance, descending.

6. f)

   t = 600, variance at end-simulation

Fig 4. Shift in the distribution of phylogenetic root ages for a) control, b) Random at μ_M = 0.75, c) selective-on-diversifiers at μ_M = 0.75, d) selective-on-relicts at μ_M = 0.75.

Coloured bars show number of replicates (vertical axis) with phylogenetic roots whose time of origin falls into the specified root age bins (horizontal axis). Distributions of root ages were recorded at the time points shown along the ‘‘time after extinction” axis (depth axis).