10.5061/DRYAD.2TG34
Legendre, Frédéric
Sorbonne University
Condamine, Fabien L.
French National Centre for Scientific Research
Data from: When Darwin’s special difficulty promotes diversification in insects
Dryad
dataset
2018
Termites
species selection
Aggregate trait
emergent trait
eusocial insects
2018-02-15T17:21:19Z
en
https://doi.org/10.1093/sysbio/syy014
11047709 bytes
1
CC0 1.0 Universal (CC0 1.0) Public Domain Dedication
Eusociality, Darwin’s special difficulty, has been widely investigated but
remains a topic of great debate in organismal biology. Eusocial species
challenge existing theories, and the impact of highly integrated societies
on diversification dynamics is controversial with opposing assertions and
hypotheses in the literature. Here, using phylogenetic approaches in
termites – the first group that has evolved eusociality – we assessed the
fundamental prediction that eusocial lineages have higher diversiﬁcation
rates than non-eusocial clades. We found multiple lines of evidence that
eusociality provided higher diversification as compared to
non-eusociality. This is particularly exacerbated for eusocial species
with ‘true’ workers as compared to species with ‘false’ workers. Because
most species with ‘true’ workers have an entirely prokaryotic microbiota,
the latter feature is also related to higher diversification rates, but it
should be investigated further, notably in relation to angiosperm
diversification. Overall, this study suggests that societies with ‘true’
workers are not only more successful at ecological timescales but also
over millions of years, which further implies that both organism- and
species-level traits act on species selection.
Figure S1 - Partitioning Isoptera finalFigure S1. Partitioning the
phylogeny of Dictyoptera into evolutionary scenarios. The null scenario is
the entire dictyopteran tree. Then each time an evolutionary scenario is
created, it consisted into a subclade and the rest of the tree composed of
all dictyopterans without the subclade (i.e. here called the backbone).
The numbers at nodes denotes all seven subclades. The first scenario
excludes the entire termite (Isoptera, node 1). The second scenario
excludes the Euisoptera (node 2). The third scenario excludes the
Kalotermitidae + Neoisoptera (node 3). The fourth scenario excludes the
Neoisoptera (node 4). The fifth scenario excludes the Neoisoptera minus
the subfamily Rhinotermitinae (node 5). The sixth scenario excludes the
Termitidae + Coptotermitinae + Heterotermitinae (node 6). The seventh
scenario excludes the family Termitidae (node 7).Figure S2 - Prior and
posterior probabilities for shiftsFigure S2. Frequency distribution of
distinct macroevolutionary rate regimes estimated for the Dictyoptera
using BAMM with a Poisson prior of 10. A scenario including five shifts of
diversification has the highest posterior probability Similar results are
obtained with different values of the Poisson prior (Fig. S6).Figure S3 -
Marginal probabilities and marginal odds ratios of the BAMM runFigure S3.
Two different metrics of weighing the relative evidence of a
diversification shift occurring along any individual branch. (a) The
phylogenetic tree has its branch lengths been replaced by the
branch-specific marginal shift probabilities, i.e. the length of a given
branch is equal to the percentage of samples from the posterior that
contain a rate shift on that particular branch. (b) The phylogenetic tree
has the branch lengths scaled to equal the corresponding marginal odds
ratio accounting for the effects of the prior and branch length. The
longest branch length, in both trees, is labelled for reference. In both
cases, the longest branch is within the termites.Figure S4 - Credible set
of diversification shifts in DictyopteraFigure S4. Credible set of
configuration shifts for net diversification of Dictyoptera inferred with
BAMM. Phylogenies show the distinct shift configurations with the highest
posterior probability. For each shift configuration, the locations of rate
shifts are shown as black circles, with circle size proportional to the
marginal probability of the shift. Text labels (e.g. f=0.11) denote the
posterior probability of each shift configuration.Figure S5 - Best shift
configuration in diversification shifts in DictyopteraFigure S5. The best
shift configuration for net diversification shifts inferred with BAMM. The
phylogeny indicates five core rate shifts (indicated by red-filled circle)
within the termites, two within the Mantodea, and two within the
cockroaches (notably in Blaberidae, Panesthiinae). The first shift in
mantises occurred early (166.8 Ma) and includes most of the mantises but
leaves out all ancient and depauperate lineages near the root of the tree.
The second shift within mantises is located at the base of a clade
including notably the plant-mimicking mantises (Empusidae), the flower
mantises (Hymenopodidae), and the core of praying mantises (Mantidae). The
first shift in cockroaches is ancient (243 Ma), just after the
Permian-Triassic extinction, corresponds to the divergence of the termite
lineage (including Cryptocercidae and Lamproblattidae, two species-poor
families of cockroaches) and the lineage leading to Blattidae. The second
shift occurred at the K-Pg event (66 Ma), and involves an offshoot of the
blaberid radiation (Panesthiinae, ca. 150 species). The most important
shift occurred within termites, 66 Ma, at the node sustaining the
radiation of Termitidae and a part of Rhinotermitidae. Interestingly this
lineage is composed only by eusocial species with true workers (Fig.
S1).Figure S6 - BAMM analyses to check for prior effectFigure S6. All the
results for the BAMM analyses using a range of values for the Poisson
prior process (0.1/0.5/1/5/10/50). The figures are ranked as follows: (1)
prior and posterior distribution, and (2) best configuration. Overall, the
results indicate a similar macroevolutionary mixture of rate shifts and
diversification rates, with a significant shift within termites and a
higher net diversification for termites.Figure S7 - Differences BiSSE
MCMCDifferences between speciation (a), extinction (b), and net
diversification rates (c), computed from the MCMC analyses using the best
BiSSE model. No posterior distribution overlaps with the red line,
indicating that the differences between all rates are significant.
Eusocial lineages diversified faster than non-eusocial lineages.Figure S8
- Differences MuSSE worker states macroevolutionary rates MCMCDifferences
in rates computed from the MCMC analyses using the best MuSSE model for
the ‘true’ workers. The compound figure shows: 1) the differences between
speciation rates as made by pair comparisons; 2) the differences between
extinction rates; and 3) the differences between net diversification
rates. Only the lineages with ‘true’ workers have a significant different
speciation, extinction, and net diversification rates (i.e. no posterior
distribution overlaps with the red line). Eusocial lineages with ‘true’
workers diversified faster than non-eusocial lineages and eusocial
lineages with pseudergates.Figure S9 - Differences MuSSE hindgut
microbiota macroevolutionary rates MCMCDifferences in rates computed from
the MCMC analyses using the best MuSSE model for the gut microbiota. The
compound figure shows: 1) the differences between speciation rates as made
by pair comparisons; 2) the differences between extinction rates; and 3)
the differences between net diversification rates. Only the lineages with
an entirely prokaryotic gut microbiota have a significant different net
diversification rates (i.e. no posterior distribution overlaps with the
red line). Eusocial lineages with an entirely prokaryotic hindgut
microbiota diversified faster than other lineages (cellulolytic
flagellates or no specialized microbiota for lignocellulose
digestion).Figure S10 - Simulations with SSE modelsRandomization tests for
(a) BiSSE, (b) MuSSE on the worker state, and (c) MuSSE on the hindgut
microbiota. The difference of fit between the best model and the reference
model is shown with the red vertical line for real data, and in vertical
coloured bars for the distribution of simulated data. The tests show that
our results are robust to type-I error.Figure S11 - MuSSE hindgut
microbiota Wood-feeding non-eusocialResults for the MuSSE analyses with
the wood-feeding non-eusocial lineages re-coded as cellulolytic
flagellates along with plots of the differences in rates computed from the
MCMC analyses using the best MuSSE model. The compound figure shows: 1)
the differences between speciation rates as made by pair comparisons; 2)
the differences between extinction rates; and 3) the differences between
net diversification rates. Only the lineages with an entirely prokaryotic
hindgut microbiota have a significant different net diversification rates
(i.e. no posterior distribution overlaps with the red line). Eusocial
lineages with an entirely prokaryotic hindgut microbiota diversified
faster than other lineages (cellulolytic flagellates or no specialized
microbiota for lignocellulose digestion).Figure S12 - MuSSE hindgut
microbiota rates MacrotermitinaeResults for the MuSSE analyses with the
Macrotermitinae re-coded with ‘lower’ termites, due to their simple
hindgut structure, along with plots of the differences in rates computed
from the MCMC analyses using the best MuSSE model. The compound figure
shows: 1) the differences between speciation rates as made by pair
comparisons; 2) the differences between extinction rates; and 3) the
differences between net diversification rates. Only the lineages with a
complex hindgut structure have a significant different net diversification
rates (i.e. no posterior distribution overlaps with the red line).
Eusocial lineages with a complex hindgut structure diversified faster than
other lineages (eusocial and non-eusocial organisms with simple hindgut
structure)Table S1 - BAMM analysesSummary of diversification models in
BAMM compared across a gradient of values for the Poison process governing
the number of rate shifts. The analyses show that a scenario with either
four, five or six shifts of diversification best explained the
macroevolution of Dictyoptera. Although it might suggest that the Poison
prior has some effect on the analyses, it is important to note that all
shifts are in common between the analyses (see Fig. S6 for more details).
Based on the effective sample size (ESS) and the highest posterior
distribution per number of shifts for the Poisson rate prior, we selected
the model with a Poison prior of 10 (highlighted in bold). In addition
this model represents an intermediary among the analyses (i.e. we did not
favour a model with more shifts or a model with few shifts).Table S2 - SSE
analysesSupports for eusociality, eusocial lineages with ‘true’ workers,
and eusocial lineages with entirely prokaryotic microbiota as driver(s) of
diversification. Tables (a), (c) and (e) report the means for each value
estimated based on 100 dated trees, for each diversification model applied
under the BiSSE approach, their number of parameters (NP), the
log-likelihood (logL), the corrected Akaike Information Criterion (AICc),
the difference of AICc (ΔAIC) between the best model (lowest AIC) and a
given model. The best model is highlighted in bold and determined by ∆AIC.
Tables (b), (d) and (f) report the standard errors for each parameter
estimated by the diversification models and listed in the tables (a), (c)
and (e).