ArticlePDF Available

Mitochondrial Phylogenomics Resolves the Global Spread of Higher Termites, Ecosystem Engineers of the Tropics

Authors:

Abstract and Figures

The higher termites (Termitidae) are keystone species and ecosystem engineers. They have exceptional biomass and play important roles in decomposition of dead plant matter, in soil manipulation, and as the primary food for many animals, especially in the tropics. Higher termites are most diverse in rainforests, with estimated origins in the late Eocene (∼54 Ma), postdating the breakup of Pangaea and Gondwana when most continents became separated. Since termites are poor fliers, their origin and spread across the globe requires alternative explanation. Here, we show that higher termites originated 42-54 Ma in Africa and subsequently underwent at least 24 dispersal events between the continents in two main periods. Using phylogenetic analyses of mitochondrial genomes from 415 species, including all higher termite taxonomic and feeding groups, we inferred 10 dispersal events to South America and Asia 35-23 Ma, coinciding with the sharp decrease in global temperature, sea level, and rainforest cover in the Oligocene. After global temperatures increased, 23-5 Ma, there was only one more dispersal to South America but 11 to Asia and Australia, and one dispersal back to Africa. Most of these dispersal events were transoceanic and might have occurred via floating logs. The spread of higher termites across oceans was helped by the novel ecological opportunities brought about by environmental and ecosystem change, and led termites to become one of the few insect groups with specialized mammal predators. This has parallels with modern invasive species that have been able to thrive in human-impacted ecosystems.
Content may be subject to copyright.
Mitochondrial Phylogenomics Resolves the Global Spread
of Higher Termites, Ecosystem Engineers of the Tropics
Thomas Bourguignon,*
,1,2,3
Nathan Lo,
3
Jan
Sobotn
ık,
2
Simon Y.W. Ho,
3
Naeem Iqbal,
4
Eric Coissac,
5,6
Maria Lee,
1
Martin M. Jendryka,
1
David Sillam-Dusse`s,
7,8
Barbora K
r
ı
zkov
a,
2
Yves Roisin,
9
and
Theodore A. Evans
1,10
1
Department of Biological Sciences, National University of Singapore, Singapore, Singapore
2
Faculty of Forestry and Wood Sciences, Czech University of Life Sciences, Prague, Czech Republic
3
School of Life and Environmental Sciences, University of Sydney, Sydney, NSW, Australia
4
Department of Plant Protection, Faculty of AgriculturalSciences,GhaziUniversity,DeraGhaziKhan,Pakistan
5
Centre National de la Recherche Scientifique, Laboratoire d’Ecologie Alpine (LECA), Grenoble, France
6
Laboratoire d’Ecologie Alpine (LECA), Universite´ Grenoble Alpes, Grenoble, France
7
Institut de Recherche pour le De´veloppement, Sorbonne Universite´s, iEES-Paris, Bondy, France
8
Universite´ Paris 13, Sorbonne Paris Cite´, LEEC, Villetaneuse, France
9
Evolutionary Biology and Ecology, Universite´ Libre de Bruxelles, Bruxelles, Belgium
10
School of Animal Biology, University of Western Australia, Perth, WA, Australia
*Corresponding author: E-mail: thomas.bourgui@gmail.com.
Associate editor: Nicolas Vidal
Abstract
The higher termites (Termitidae) are keystone species and ecosystem engineers. They have exceptional biomass and play
important roles in decomposition of dead plant matter, in soil manipulation, and as the primary food for many animals,
especially in the tropics. Higher termites are most diverse in rainforests, with estimated origins in the late Eocene
(54 Ma), postdating the breakup of Pangaea and Gondwana when most continents became separated. Since termites
are poor fliers, their origin and spread across the globe requires alternative explanation. Here, we show that higher
termites originated 42–54 Ma in Africa and subsequently underwent at least 24 dispersal events between the continents
in two main periods. Using phylogenetic analyses of mitochondrial genomes from 415 species, including all higher
termite taxonomic and feeding groups, we inferred 10 dispersal events to South America and Asia 35–23 Ma, coinciding
with the sharp decrease in global temperature, sea level, and rainforest cover in the Oligocene. After global temperatures
increased, 23–5 Ma, there was only one more dispersal to South America but 11 to Asia and Australia, and one
dispersal back to Africa. Most of these dispersal events were transoceanic and might have occurred via floating
logs. The spread of higher termites across oceans was helped by the novel ecological opportunities brought about
by environmental and ecosystem change, and led termites to become one of the few insect groups with specialized
mammal predators. This has parallels with modern invasive species that have been able to thrive in human-
impacted ecosystems.
Key words: historical biogeography, insects, Isoptera.
Introduction
Termites have a nearly global distribution and comprise
3,000 described species (Krishna et al. 2013). Despite their
modest levels of diversity, they are among the most successful
terrestrial organisms on the earth in terms of sheer abun-
dance, making up 10–20% of the animal biomass in tropical
ecosystems worldwide (Eggleton et al. 1996;Ellwood and
Foster 2004). The success of termites is in large part due to
their ability to digest lignocellulose, the most abundant or-
ganic molecule on earth, and dissolved organic molecules in
soil (Norkrans 1963;Dixon et al. 1994). They play an essential
role in decomposition and nutrient recycling, consuming up
to 90% of wood, dead plant matter, and soil organic matter in
some habitats (Bignell 2006;Jouquet et al. 2011,2016).
Termitesmovetonnesofsoilperhectareperyearandare
considered ecosystem engineers (Jouquetetal.2016). Their
abundance has also allowed termites and ants to become the
only insect groups with specialist mammalian predators
(Redford 1987).
The “higher” termites (family Termitidae) constitute the
vast majority of termite species (80%) and are the most
ecologically dominant taxa. Although termites are commonly
thought to feed primarily on wood, termitids consume a
variety of organic matter and more than half of the species
feed on soil. The evolutionary history of this important and
dominant group, which spans across several biogeographic
Article
ßThe Author 2016. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
All rights reserved. For permissions, please e-mail: journals.permissions@oup.com
Mol. Biol. Evol. 34(3):589–597 doi:10.1093/molbev/msw253 Advance Access publication December 25, 2016 589
regions, is likely to have been complex. The termite fossil
record dates back to 140 Ma (Engel et al. 2007), but a recent
molecular analysis of 66 termite species placed the origin of
Termitidae at only 54 Ma (Bourguignon et al. 2015). For this
reason, the origin of Termitidae is believed to postdate the
breakup of Pangaea and Gondwana. Because termites are
weak flyers (Hu et al. 2007), they are expected to be poor
dispersers and the origin of their global distribution is enig-
matic. While vicariance played a critical role in the early di-
versification of termites (Bourguignon et al. 2015), the extent
to which termitids dispersed across oceans remains poorly
understood.
The poor fossil record of Termitidae (Engel et al. 2009)has
left considerable uncertainty about how and when this group
dispersed to the major landmasses. This question can be ad-
dressed in detail using molecular phylogenies inferred from a
worldwide sample of termitids. Although some studies have
included extensive taxon samples (Inward et al. 2007;
Legendre et al. 2015) and others have used large amounts
of sequence data (Cameron et al. 2012;Bourguignon et al.
2015), no studies have yet combined these two features.
To resolve the historical biogeography of higher termites,
we analyzed full mitochondrial genomes from 415 species,
including 384 termitids, representing 18% of the described
species (supplementary tables S1 and S2,Supplementary
Material online). These termites were sampled from 13 coun-
tries in Africa, Asia, South America, and Australia. By including
age calibrations from 15 fossils (supplementary table S3,
Supplementary Material online), we estimated the evolution-
ary timeframe of the group. Our specific aims were to deter-
mine: (1) the geographic origin of higher termites; (2) the
pathways and timing of dispersal events; and (3) whether
dispersal events coincided with major climatic changes and
with the origin of termite-specific predators.
Results and Discussion
Origin of Higher Termites
Our estimate of the evolutionary timescale shows that mod-
ern higher termites originated in Africa 47.6 Ma (95% cred-
ibility interval: 42.2–53.7 Ma) (fig. 1). This is consistent with
African rainforests harboring the highest diversity of
Termitidae, and comprising most of the earliest-branching
lineages in the group (Eggleton 2000). Our estimate was ob-
tained after excluding third codon positions and using the
best-fitting clock model. However, we obtained consistent
results when we repeated the analysis with and without third
codon positions, using different clock models and phylogen-
etic methods, and using different methods for reconstructing
ancestral ranges (supplementary figs. S1–S6,Supplementary
Material online).
Eocene–Oligocene out of Africa
We inferred at least five dispersals of higher termites to South
America and five dispersals to Asia, towards the end of the
Eocene through to the Oligocene, 35–23 Ma (figs. 2 and 3).
Five of these dispersal events were from Africa and five were
from undetermined origins. The inception of the “out of
Africa” dispersals of higher termites coincides with a sharp
drop in the atmospheric concentration of carbon dioxide
(Pagani et al. 2005) and in the global temperature at the
Eocene–Oligocene boundary, 34 Ma, as inferred from deep-
sea oxygen isotopic ratios (Zachos et al. 2001), which triggered
a mass extinction. Global temperatures remained consistently
low until the end of the Oligocene (Zachos et al. 2001), trig-
gering the retraction of megathermal rainforests towards the
equator, where they survived as tropical rainforests, albeit
experiencing numerous extinctions (fig. 3)(Morley 2011).
Termitids therefore colonized Asia and South America during
major reworking of tropical ecosystems, at the time when
tropical rainforests acquired their modern flora (Morley
2011)(fig. 2).
New Dispersal Patterns during the Miocene
Our ancestral range reconstruction shows a change in disper-
sal patterns during the Miocene, 23.0–5.3 Ma, once tempera-
tures had increased (Zachos et al. 2001). Higher termites
dispersed only once to South America and 6 times to Asia.
They also dispersed once, and for the first time, to Africa from
Asia, and 5 times to Australia.
The low rate of colonization of South America compared
with Asia in the Miocene can be explained by a combination
of ecological and tectonic factors. Termitids were already
abundant and diverse in the Dominican amber 14–
20 Ma (Krishna and Grimaldi 2009), suggesting that they
rapidly diversified following their arrival in South America,
preventing later establishments of ecologically similar species.
Although a similar situation is likely to have existed in Asia,
the Gomphotherium land bridge created a terrestrial connec-
tion between Africa and Eurasia during the early Miocene
18–20 Ma (Ro¨gl 1998,1999). This land bridge is likely to
have allowed the fungus-growing macrotermitine termites to
crossfromAfricatoAsiaatthistime(Aanen and Eggleton
2005), given that this group did not reach either South
America or Australia, neither of which had land bridges
with Africa.
Australia was colonized by at least five lineages, once from
Asia, once from South America and thrice from undeter-
mined regions. The Occasitermes lineage was the first to ar-
rive, at latest 19.8 Ma, followed by four more lineages that
dispersed to Australia during a short time period, 11–13 Ma.
This timing coincides with a sharp increase in aridification,
14 Ma, and the expansion of the arid biome in Australia,
during the second half of the Miocene, 15–5.3 Ma
(Martin 2006). The expansion of the arid biome and its sclero-
phyll vegetation offered ecological opportunities for new
groups to diversify and take over ecosystem functions
(Crisp and Cook 2013). Today, higher termites are the dom-
inant decomposers in the arid biome (Abensperg-Traun and
Steven 1997).
Higher Termites Dispersed between Biogeographic
Regions by Rafting
The Gomphotherium land bridge between Asia and Africa
possibly explains the colonization of Africa by
Pericapritermes from Asia. It may explain the colonization
Bourguignon et al. .doi:10.1093/molbev/msw253 MBE
590
of Asia by Microtermes,Ancistrotermes pakistanicus,
Odontotermes and Macrotermes. The last two of these genera
might be restricted to land dispersal because of their fungus-
growing behaviour (Nobre et al. 2010). It also potentially ex-
plains other colonizations of Asia, by Microcerotermes and
Termes, which dispersed from Africa, possibly after Asia and
Africa became connected by land. Alternatively, these disper-
sal events might have been by rafting in wood pieces over
water, as it must have been for the other 17 dispersal events.
Given the poor flight capability of termites, it seems likely that
termites dispersed by rafting in wood, probably logs from
trees (Bourguignon et al. 2016). This would suggest that the
dispersing termites were wood feeding, and that other feeding
habits evolved after dispersal (Inward et al. 2007). However,
our results show that extant species of some early branching
lineages are soil feeding for some comparisons, such as in the
South American Apicotermitinae and Syntermitinae. There
are two possible explanations: either that the dispersing spe-
cies were wood-feeding and are now extinct, or that soil
feeders dispersed across oceans, possibly in arboreal nests
attached to floating trees. There are modern soil-feeding,
tree-nesting species in these families, e.g., Anoplotermes
banksi and Labiotermes labralis.
Higher Termites Colonized New Continents during
Environmental Changes
Our study shows that the timing of higher termite dispersals
coincides with the opening of ecological opportunities due to
climate change. Higher termites originated in Africa and dis-
persed from there in two phases. The first phase was initiated
by the retraction of megathermal rainforests to the equatorial
region at the end of the Eocene, 34 Ma (Morley 2011).
FIG.1.Bayesian phylogenetic tree of higher termites inferred from complete mitochondrial genomes, with third codon positions excluded.
The tree is drawn to a time scale given in millions of years. Node bars represent the 95% credibility intervals of node-time estimates.
Branches are labelled with posterior probabilities. Circles show the ancestral distribution inferred for each node using a Bayesian phylo-
genetic analysis. Clades comprising species from a single biogeographic area are collapsed into triangles. Internal branches and ancestral
states are shown in colour only when the posterior probability of the ancestral reconstruction is >0.95. The map shows the four areas
considered in the analyses.
Mitochondrial Phylogenomics Resolves the Global Spread of Higher Termites .doi:10.1093/molbev/msw253 MBE
591
The second phase coincided with the expansion of the arid
biome in Australia during the middle Miocene, 14 Ma (Martin
2006).
Based on the evidence presented earlier, we hypothesize
that termites colonized multiple continents as they were
undergoing major environmental and climatic changes.
Ecosystems undergoing such changes may be more vulner-
able to biological invasion (Elmqvist et al. 2003;Davis 2009).
This has parallels with the success of modern invasive species
in ecosystems disturbed by human activities (King and
Tschinkel 2008). We detected one recent and unusual disper-
sal event 1.2 Ma (Holocene), Ancistrotermes pakistanicus dis-
persing from the African equatorial rainforest to tropical Asia.
Given the long connection between these continents, it
seems possible that (ancient) humans assisted this recent
dispersal as they have with many other termites (Evans
et al. 2013).
Influence of Higher Termite Arrival on Mammal
Predators
There is a possibility that the evolution of termites influ-
enced the evolution of other species, especially their
predators. The only groups of insects with specialist mam-
malian predators are termites and ants. As many myrme-
cophagous mammals eat both of these insect taxa, there
is a question whether these mammals evolved to eat ter-
mites first, then expanded to ants, or vice versa. We found
that of the six mammals that eat only termites, five
evolved after the appearance of the termite genera
upon which they prey (fig. 4).Thesoleexception,the
FIG.2. Graph summarizing dispersals between biogeographic areas. The upper curve represents the minimum partial pressure of atmospheric
CO
2
as in Pagani et al. (2005). The lower curve represents deep-sea oxygen isotope records as in Zachos et al. (2001), whereby lower values
indicate warmer climate. Circles represent the maximum estimated age of the dispersal, given by the mean posterior estimates of the timing of
divergence from the most closely related foreign taxon, based on a Bayesian phylogenetic analysis. Only the dispersals with posterior prob-
ability exceeding 0.95 in all analyses are shown. Circles are coloured when the provenance of dispersers was retrieved in all analyses with a
posterior probability exceeding 0.95. Blue: Africa; red: South America; green: Asia. Blue bars represent the 95% credibility intervals of the age
estimates.
Bourguignon et al. .doi:10.1093/molbev/msw253 MBE
592
numbat in Australia, has no close relatives and its timing
of origination might be overestimated by comparison
with its sister lineage in the mammal tree (dos Reis
et al. 2012). Five of 10 mammals that eat termites and
ants evolved after their termite prey. As this is the pattern
observed for the termite specialists, we suggest that they
evolved to eat termites first, then added ants to their diet
later. The other five mammal species evolved before their
termite prey, possibly adapting from an ant-based diet or
general insectivory (as suggested by armadillos in South
America and mongooses in Africa; supplementary table
S4,Supplementary Material online). Note that the esti-
mated timing of the origin of pangolins, like numbats,
suffers from a lack of close relatives (dos Reis et al.
2012). Although not definitive, our data show that the
arrival of termites predates mammalian myrmecophagy,
which suggests that termites promoted the diversification
of insectivorous mammals. This idea could be tested with
a phylo-biogeographical study on other prey species, es-
pecially ants. Further study of other predators may find
clearer patterns, confirming the major impacts that
termites have had on their ecosystems as keystone spe-
cies, as ecosystem engineers, and as the major decom-
posers of the tropics.
Materials and Methods
Mitochondrial Genome Sequencing
We carried out worldwide sampling of higher termites (family
Termitidae) and sequenced complete mitochondrial gen-
omes from 346 samples. In combination with 38 samples
sequenced in previous studies, we assembled a data set com-
prising 384 species (supplementary table S1,Supplementary
Material online). To infer the position of the root in our
phylogenetic analysis, we included the mitochondrial gen-
omes of 30 species downloaded from GenBank. These
included 25 lower termites, two cockroaches, one mantid,
one stick insect, and one grasshopper (supplementary table
S2,Supplementary Material online). All specimens were
sampled in RNA-later
V
R
and stored at 80 CuntilDNA
extraction.
We extracted whole genomic DNA from about five
individuals, from which the digestive tract was removed,
FIG.3. Timing of the major phases of dispersal by higher termites during the Cenozoic. The black arrows on the left maps show the directions of
dispersal events. The green areas on the right maps show the estimated distribution of tropical rainforests (Morley 2011). The distribution of
landmasses is as inferred by Zachos et al. (2001).
Mitochondrial Phylogenomics Resolves the Global Spread of Higher Termites .doi:10.1093/molbev/msw253 MBE
593
using phenol-chloroform extraction procedure. The com-
plete mitochondrial genomes were amplified with
TaKaRa LA Taq in two long-PCR reactions using the pri-
mers described by Bourguignon et al. (2015). We mixed
the two PCR fragments in equimolar concentration, then
multiplexed and paired-end sequenced them with
Illumina HiSeq2000.
We de novo assembled separately 88-bp paired-end reads
using the organelle assembler ORG.asm (available at http://
metabarcoding.org/asm). Each resulting assembly was then
checked by read mapping with the CLC Assembly Cell suite
of programs. ORG.asm failed to assemble 30% of the mito-
chondrial genomes, which were mapped to reference gen-
omes and assembled using the CLC Assembly Cell suite of
FIG.4. The timing of the origins of termite-eating mammals and their termite prey: (a) mammals that specialize on termites only; (b) mammals
that specialize on ants and termites. The shaded area indicates that the origin of termite prey antedates that of the mammal predators, suggesting
that the mammals evolved to eat the termites. The number of termite origin dates (horizontal standard error bars) varies between mammals. A
mammal species has either one termite origin date if it targets just one termite genus or subfamily (e.g., aardwolves and Trinervitermes), or two
termite origin dates if it eats many (the two origin dates are for the most commonly eaten termite species). See supplementary table S4,
Supplementary Material online, for the complete list of termite prey.
Bourguignon et al. .doi:10.1093/molbev/msw253 MBE
594
programs. Briefly, reads were mapped onto the mitochondrial
genomes of closely related species that served as references.
The sequence of the reference was then replaced by the con-
sensus inferred from the reads. In all cases of polymorphic
bases, we selected the base with the highest representation.
Reads were mapped again onto the new consensus sequence,
and this procedure was repeated until we reached stability.
We inspected by eye all assembled mitochondrial genomes,
with the reads mapped onto them.
We omitted control regions of the mitochondrial genomes
from the final matrix, as they present repetitive patterns that
are generally poorly assembled with short reads, and thus
provide no useful information. We annotated the 22 tRNA
genes, the 13 protein-coding genes, and the two ribosomal
RNA genes by manual checking, aided by previously pub-
lished sequences that we aligned to each mitochondrial gen-
omeusingtheMusclealgorithmimplementedinMEGA5.2.1
(Tamura et al. 2011), taking into account the codon structure
of the protein-coding genes. The resulting sequence align-
ments were concatenated with SequenceMatrix (Vaidya
et al. 2011).
Phylogenetic Analyses and Molecular Dating
We partitioned the sequence alignment into five subsets:
one for each codon position of the concatenated protein-
coding genes, one for the 12S and 16S rRNA genes, and
oneforthetRNAgenes.Wefoundnoevidenceofsatur-
ation at the third codon positions of the protein-coding
genes using Xia’s method in DAMBE (NumOTU ¼32,
I
SS
¼0.478, I
SS.C
Asym ¼0.517) (Xia et al. 2003;Xia and
Lemey 2009). However, we detected heterogeneity in
base composition between samples at the third codon
positions (chi-square ¼11771.72; df ¼672; P<10
6
).
Therefore, we ran each analysis with and without the
third codon positions, giving preference to the analyses
in which the third codon positions were excluded. This
strategy allowed us to determine the impact of base com-
positional heterogeneity at third codon positions on our
estimates of the tree topology and evolutionary timescale.
We analyzed the concatenated sequence alignment using
the Bayesian phylogenetic software BEAST 1.8.0 (Drummond
and Rambaut 2007). For each subset of the data, we assigned
an independent GTR model of nucleotide substitution with
gamma-distributed rate variation across sites. We imple-
mented two models of rate variation across branches: a strict
clock and an uncorrelated lognormal relaxed clock
(Drummond et al. 2006). In both of these models, we allowed
each subset of the data to have a distinct relative rate. In both
the analyses with and without third codon positions, com-
parison of the marginal likelihood indicated decisive support
for the uncorrelated lognormal relaxed clock over the strict
clock. Therefore, we only present the trees inferred using an
uncorrelated lognormal relaxedclock.Abirthdeathspeci-
ation process was used for the tree prior (Gernhard 2008).
The molecular clock was calibrated using 15 minimum
age constraints (supplementary table S3,Supplementary
Material online). These constraints were based on the
fossil record, and we systematically selected the youngest
possible age for each fossil as mentioned on the
Paleobiology Database (www.paleobiodb.org; last ac-
cessed on 15 July 2015). Fossil calibrations were imple-
mented as exponential priors on node times (Ho and
Phillips 2009). We allowed the calibrated nodes to be
considerably older than the oldest known fossils because
the termite fossil record is fragmentary and often under-
estimates node age (Ho and Phillips 2009). We chose the
values for the 97.5% soft maximum bounds based on a
combination of phylogenetic bracketing and absence of
fossil evidence (supplementary table S3,Supplementary
Material online).
Posterior distributions of parameters, including the
tree, were estimated using Markov chain Monte Carlo
(MCMC) sampling. We performed three replicate
MCMC runs, with the tree and parameter values sampled
every 20,000 steps over a total of 200 million generations
in each case. Acceptable sample sizes and convergence to
the stationary distribution were checked using Tracer 1.5
(Rambaut and Drummond 2007), with a proportion of
samples removed as burn-in. The remaining samples
from the three MCMC runs were combined and the
maximum-clade-credibility tree was obtained using
TreeAnnotator in BEAST.
To test the sensitivity of our estimates to the choice of
phylogenetic method, we also analyzed the concatenated
sequence alignment using maximum likelihood in RAxML
version 7.7.1 (black-box webserver; http://embnet.vital-it.ch/
raxml-bb/) (Stamatakis et al. 2008). We used a gamma distri-
bution to model rate heterogeneity across sites. Node support
was estimated using 100 bootstrap replicates. We ran analyses
with and without the third codon positions of the protein-
coding genes.
Biogeographic Analyses
We reconstructed the evolution of termite geographic ranges
as a discrete trait using a Bayesian phylogenetic approach in
BEAST 1.8.0 (Drummond and Rambaut 2007). This method
reconstructs the ancestral range as a trait on each tree during
the MCMC, taking into account phylogenetic uncertainty.
We used sample locations to assign a biogeographic area to
each tip. We distinguished four biogeographic areas: Africa,
Australia, South America, and Asia.
We also reconstructed the evolution of termite geographic
ranges using a Bayesian binary model implemented in RASP
2.1 (Yu et al. 2015). We used a fixed (JC) model of state
frequencieswithequalratesacrosssites.Theanalysiswas
performed with the default chain parameters (10 chains of
50,000 steps, with samples drawn every 100 steps and with a
temperature of 0.1). Using an estimated model of state fre-
quencies and gamma-distributed rates across sites did not
substantially change the results. The root distribution was
set to Null and the maximum number of areas for each
node was set to 1. These analyses were carried out for the
trees inferred in our BEAST analysis using the uncorrelated
lognormal relaxed clock, and for the trees inferred using
RAxML.
Mitochondrial Phylogenomics Resolves the Global Spread of Higher Termites .doi:10.1093/molbev/msw253 MBE
595
Supplementary Material
Supplementary figures S1–S6 and tables S1–S4 are available at
Molecular Biology and Evolution online.
Acknowledgments
We are grateful to Tamara Hartke for providing specimens,
and to Jan K
re
cek for help with species identification. This
work was supported by the LHK fund of the National
University of Singapore; by the Singapore-MIT Alliance for
Research and Technology; by the Alliance National
University of Singapore—Universite´ Sorbonne Paris Cite´; by
the Czech Science Foundation (project No. 15-07015Y); by
the Internal Grant Agency of Faculty of Forestry and Wood
Sciences, CULS (IGA A11/16); and by the Grand Agency of the
Czech University of Life Sciences (project CIGA No.
20154320). T.B. was supported by the University of Sydney
through a postdoctoral fellowship.
References
Aanen DK, Eggleton P. 2005. Fungus-growing termites originated in
Africanrainforest.Curr Biol. 15:851–855.
Abensperg-Traun M, Steven DE. 1997. Latitudinal gradients in the spe-
cies richness of Australian termites (Isoptera). AustJEcol.
22:471–476.
Bignell DE. 2006. Termites as soil engineers and soil processors. In Ko¨nig
H, Varma A, editors. Intestinal microorganisms of termites and other
invertebrates. Berlin: Springer-Verlag. p. 183–220.
BourguignonT,LoN,CameronSL,
Sobotn
ık J, Hayashi Y, Shigenobu S,
Watanabe D, Roisin Y, Miura T, Evans TA. 2015. The evolutionary
history of termites as inferred from 66 mitochondrial genomes. Mol
Biol Evol. 32:406–421.
Bourguignon T, Lo N,
Sobotn
ık J, Sillam-Dusse`s D, Roisin Y, Evans TA.
2016. Oceanic dispersal, vicariance and human introduction shaped
the modern distribution of the termites Reticulitermes,Heterotermes
and Coptotermes.Proc R Soc Lond B 283:20160179.
Cameron SL, Lo N, Bourguignon T, Svenson GJ, Evans TAA. 2012.
mitochondrial genome phylogeny of termites (Blattodea:
Termitoidae): robust support for interfamilial relationships and
molecular synapomorphies define major clades. Mol Phylogenet
Evol. 65:163–173.
Crisp MD, Cook LG. 2013. How was the australian flora assembled over
the last 65 Million years? A molecular phylogenetic perspective.
Annu Rev Ecol Evol Syst. 44:303–324.
Davis MA. 2009. Invasion biology. Oxford: Oxford University Press.
Dixon RK, Brown S, Houghton RA, Solomon AM, Trexler MC,
Wisniewski J. 1994. Carbon Pools and flux of global forest ecosys-
tems. Science 263:185–190.
dos Reis M, Inoue J, Hasegawa M, Asher RJ, Donoghue PCJ, Yang Z. 2012.
Phylogenomic datasets provide bothprecisionandaccuracyinesti-
mating the timescale of placental mammal phylogeny. Proc R Soc
Lond B 279:3491–3500.
Drummond AJ, Ho SYW, Phillips MJ, Rambaut A. 2006. Relaxed phylo-
genetics and dating with confidence. PLoS Biol. 4:e88.
Drummond AJ, Rambaut A. 2007. BEAST: Bayesian evolutionary analysis
by sampling trees. BMC Evol Biol. 7:214.
Eggleton P, Bignell DE, Sands WA, Mawdsley NA, Lawton JH, Wood TG,
Bignell NC. 1996. The diversity, abundance and biomass of termites
under differing levels of disturbance in the Mbalmayo Forest Reserve,
southern Cameroon. Philos Trans R Soc Lond B 351:51–68.
Eggleton P. 2000. Global patterns of termite diversity. In: Abe T, Bignell
DE, Higashi M, editors. Termites: evolution,sociality,symbioses,ecol-
ogy.Dordrecht:KluwerAcademicPublishers.p.2551.
Ellwood MDF, Foster WA. 2004. Doubling the estimate of invertebrate
biomass in a rainforest canopy. Nature 429:549–551.
Elmqvist T, Folke C, Nystro¨m M, Peterson G, Bengtsson J, Walker B,
Norberg J. 2003. Response diversity, ecosystem change, and resili-
ence. Front Ecol Environ. 1:488–494.
Engel MS, Grimaldi DA, Krishna K. 2007. Primitive termites from the
early cretaceous. Stuttgarter Beitrage Zur Naturkd 371:1–32.
Engel MS, Grimaldi DA, Krishna K. 2009. Termites (Isoptera): their phyl-
ogeny, classification, and rise to ecological dominance. Am Museum
Novit. 3650:1–27.
Evans TA, Forschler BT, Grace JK. 2013. Biology of invasive termites: a
worldwide review. Annu Rev Entomol. 58:455–474.
Gernhard T. 2008. The conditioned reconstructed process. JTheorBiol.
253:769–778.
Ho SYW, Phillips MJ. 2009. Accounting for calibration uncertainty in
phylogenetic estimation of evolutionary divergence times. Syst Biol.
58:367–380.
Hu J, Zhong JH, Guo MF. 2007. Alate dispersal distances of the black-
winged subterranean termite Odontotermes formosanus (Isoptera:
Termitidae) in southern China. Sociobiology 50:1–8.
Inward DJG, Vogler AP, Eggleton P. 2007. A comprehensive phylogenetic
analysis of termites (Isoptera) illuminates key aspects of their evo-
lutionary biology. Mol Phylogenet Evol. 44:953–967.
Jouquet P, Bottinelli N, Shanbhag R, Bourguignon T, Traore´ S, Abbasi SA.
2016. Termites: the neglected engineers of tropical soils. Soil Sci.
181:157–165.
Jouquet P, Traore´ S, Choosai C, Hartmann C, Bignell D. 2011. Influence of
termites on ecosystem functioning. Ecosystem services provided by
termites. Eur J Soil Biol. 47:215–222.
King JR, Tschinkel WR. 2008. Experimental evidence that human impacts
drive fire ant invasions and ecological change. Proc Natl Acad Sci
USA. 105:20339–20343.
Krishna K, Grimaldi D. 2009. Diverse Rhinotermitidae and
Termitidae (Isoptera) in Dominican amber. Am Museum
Novit. 3640:1–48.
Krishna K, Grimaldi DA, Engel MS. 2013. Treatise on the Isoptera of the
World: Vol. 1. Bull Am Museum Nat Hist. 377:1–196.
Legendre F, Nei A, Svenson GJ, Robillard T, Pellens R, Grandcolas P. 2015.
Phylogeny of Dictyoptera: dating the origin of cockroaches, praying
mantises and termites with molecular data and controlled fossil
evidence. PLoS One 10:e0130127.
Martin HA. 2006. Cenozoic climatic change and the development of the
arid vegetation in Australia. JAridEnviron. 66:533–563.
Morley RJ. 2011. Cretaceous and Tertiary climate change and the past
distribution of megathermal rainforests. In: Bush MB, Flenley J,
Gosling WD, Morley RJ, editors. Tropical rainforest responses to
climaticchange.Chichester:Springer.p.134.
Nobre T, Eggleton P, Aanen DK. 2010. Vertical transmission as the key to
the colonization of Madagascar by fungus-growing termites?. Proc R
Soc Lond B 277:359–365.
Norkrans B. 1963. Degradation of cellulose. Annu Rev Phytopathol.
1:325–350.
Pagani M, Zachos JC, Freeman KH, Tipple B, Bohaty S. 2005. Marked
decline in atmospheric carbon dioxide concentrations during the
Paleogene. Science 309:600–604.
Rambaut A, Drummond AJ. 2007. Tracer v. 1.6. Last accessed on
February 2016. Available from: http://beast.bio.ed.ac.uk/Tracer.
Redford KH. 1987. Ants and termites as food. Patterns of mammalian
myrmecophagy. Curr Mammal. 1:349–399.
Ro¨gl F. 1999. Mediterranean and paratethys. Facts and hypotheses of an
Oligocene and Miocen paleogeography (short review). Geol
Carpathica. 50:339–349.
Ro¨gl VF. 1998. Palaeogeographic considerations for Mediterranean and
Paratethys seaways (oligocene to miocene). Ann Naturhist Mus Wien
99A:279–310.
Stamatakis A, Hoover P, Rougemont J. 2008. A rapid bootstrap algorithm
for the RAxML Web servers. Syst Biol. 57:758–771.
Tamura K, Peterson D, Stecher G, Nei M, Kumar S. 2011. MEGA5: mo-
lecular evolutionary genetics analysis using maximum likelihood,
evolutionary distance, and maximum parsimony methods. Mol
Biol Evol. 28:2731–2739.
Bourguignon et al. .doi:10.1093/molbev/msw253 MBE
596
Vaidya G, Lohman DJ, Meier R. 2011. SequenceMatrix: concatenation
software for the fast assembly of multi-gene datasets with character
set and codon information. Cladistics 27:171–180.
Xia X, Lemey P. 2009. Assessing substitution saturation with
DAMBE. In: Lemey P, Salemi M, Vadamme A, editors. The
phylogenetic handbook: a practical approach to DNA and pro-
tein phylogeny. United Kingdom: Cambridge University Press.
p. 615–630.
Xia X, Xie Z, Salemi M, Chen L, Wang Y. 2003. An index of substitution
saturation and its application. Mol Phylogenet Evol. 26:1–7.
Yu Y, Harris AJ, Blair C, He X. 2015. RASP (Reconstruct Ancestral State in
Phylogenies): a tool for historical biogeography. Mol Phylogenet Evol.
87:46–49.
ZachosJ,PaganiM,SloanL,ThomasE,BillupsK.2001.Trends,rhythms,
and aberrations in global climate 65 Ma to present. Science
292:686–694.
Mitochondrial Phylogenomics Resolves the Global Spread of Higher Termites .doi:10.1093/molbev/msw253 MBE
597
View publication statsView publication stats
... Asymmetrical snappers appeared separately in the Old World (Pericapritermes and related genera), in Madagascar (Capritermes) and in the Neotropics, where Inward et al. (2007) suggested that they evolved independently twice, once in Planicapritermes and once in Neocapritermes. Although more recent studies have established a close relationship between Planicapritermes and Neocapritermes, forming the sister clade to the symmetrical snapper Crepititermes (Bourguignon et al. 2017), it remains that asymmetrical snapping must also have evolved independently in the neotropical Termes group (Dihoplotermes and probably Cornicapritermes). Bourguignon et al.'s (2017) study included a taxon from French Guiana provisionally labelled "G683 Neocapritermes sp. ...
... Complete mitochondrial DNA sequences have now confirmed the close relationship between Neocapritermes and Planicapritermes (Bourguignon et al. 2017), as proposed by earlier authors (Krishna 1968;Constantino 1998) but in contrast with the preferred tree of Inward et al. (2007), in which Planicapritermes joined a morphologically and zoogeographically improbable lineage including Orthognathotermes and Globitermes; however, several nodes among the Termitinae were weakly supported, and Inward et al. (2007) did not discard the possible monophyly of Neocapritermes + Planicapritermes. This new genus Schievitermes clearly belongs in the Neocapritermes + Planicapritermes clade, in which it seems to come closer to Planicapritermes in accordance with morphological and anatomical characters. ...
... Worker's mtDNA sequence deposited in GenBank under label Neocapritermes sp. H TB-2017 isolate G683, accession KY224444(Bourguignon et al. 2017). From other colonies than holotype: French Guiana, Laussat (N1 road, PK194), forest on ...
Article
Full-text available
Asymmetrical snapping mandibles have evolved several times in termites. In the Neotropics, asymmetrical snapping mandibles are found in soldiers of four genera: Neocapritermes , Planicapritermes , Cornicapritermes and Dihoplotermes . Here, I describe Schievitermes globicornis , new genus and species, from French Guiana. This genus is characterized by an absence of a frontal prominence and slightly asymmetrical mandibles in the soldier caste. The morphology and anatomy of the worker reveal a wood-based diet, and suggest that Schievitermes , Planicapritermes and Neocapritermes constitute a monophyletic group, which is consistent with mtDNA data.
... As evidenced by recent phylogenies (Arab et al. 2017;Bourguignon et al. 2017), Nasutitermes is a heterogeneous assemblage of species, including evolutionary distant lineages from the type-species, Nasutitermes corniger (Motschulsky, 1855), not fitting into the current recognized morphological concept of the genus (sensu Mathews 1977;Sands 1965Sands , 1998. Particularly, many Neotropical Nasutitermes species are in need of complete taxonomic revision, considering especially the worker gut coiling and enteric valve morphology. ...
... previously published sequences at GenBank (Dietrich & Brune 2016;Bourguignon et al. 2017) and the BOLD platform (http://v3.boldsystems.org) to reduce missing information for both, COI and 16S. ...
... GenBank accession numbers for all used sequences are available in Table 1. Agnathotermes crassinasus Constantino, 1990 French Guiana, Petit Saut: G728 KY224404 KY224404 Bourguignon et al. 2017 Agnathotermes glaber (Snyder, 1926) Brazil, MG: MZUSP 23746 ...
Article
A new monotypic nasute termite genus, Hyleotermes gen. nov., is proposed for Nasutitermes brevipilus Emerson, 1925. Hyleotermes brevipilus, comb. nov., is redescribed and illustrated based on the morphology of the imago, soldier, and worker castes. It is expanded into Amazonia. The soldier of Hyleotermes differs from that of Nasutitermes Dudley, 1890 in that the former has a long and cylindrical nasus and the head capsule lacks long setae and is covered with microscopic setae. Unlike the worker of Nasutitermes, the Hyleotermes worker has a short mixed segment and an enteric valve is adorned with narrow spines on conical bases. The phylogenetic position of H. brevipilus comb nov., is reconstructed based on a dataset with two mitochondrial markers (COI and 16SrRNA) for 36 terminals, under maximum likelihood and Bayesian inference. Results corroborate that this species is unrelated to Nasutitermes and should be excluded from the genus.
... We built a phylogenetic tree of termites using mitochondrial genomes retrieved from metagenome assemblies. Mitochondrial contigs derived from termites were identified using BLAST search (sequence length > 5000 and percent identity > 90) [4] against previously published whole mitochondrial genomes of termites [13][14][15]146]. Mitochondrial genomes were complete or near-complete in most cases. ...
... The fossil calibrations were implemented as exponential priors on node times. Because transcriptome-based phylogenies unambiguously support the monophyly of Sphaerotermitinae and Macrotermitinae [27] (unlike mitochondrial genome-based phylogenies [15];), we constrained Sphaerotermitinae + Macrotermitinae to be monophyletic. Similarly, we constrained non-Stylotermitidae Neoisoptera to form a monophyletic group. ...
... On the other hand, the boreotropical and Gomphotherium dispersal scenarios assume younger lineage age and suggest the pivotal role of forest corridors in driving biotic exchange between Africa and Asia. For example, out-of-Africa migrations via the Gomphotherium corridor have been well documented for tetrapods (Harzhauser et al., 2007) and snakes (Pook et al., 2009), while Asia-to-Africa dispersals through the same corridor have been proposed for termites (Bourguignon et al., 2017), butterflies (Kaliszewska et al., 2015;Toussaint et al., 2019Toussaint et al., , 2021, amphibians (Yuan et al., 2018) and lizards (Tamar et al., 2016(Tamar et al., , 2018. However, it is still unclear whether these four scenarios can sufficiently explain all cases of disjunct Paleotropical distributions. ...
... (Morley, 2007;Pound et al., 2012). The existence of this corridor is used to explain the migrations of tropical biotas between Africa and Asia in both directions (Bourguignon et al., 2017;Cruaud et al., 2011;Toussaint et al., 2019Toussaint et al., , 2021Zhou et al., 2012). The Gomphotherium corridor likely existed between 27 and 14 Ma but these dates are still debated (Hamon et al., 2013;Pirouz et al., 2017;Rögl, 1999 ...
Article
Paleotropical clades with largely disjunct distributions are ideal models for biogeographic reconstructions. The dung beetle genera Grebennikovius Mlambo, Scholtz & Deschodt, Epactoides Olsouffief and Ochicanthon Vaz-de-Mello are distributed in Tanzania, Mada-gascar and Réunion, and the Oriental region, respectively. We combine morphology and molecular dataset to reconstruct the phylogenetic relationships between these taxa. Our analyses corroborate previous hypotheses of monophyly of the group, which is here described as new tribe Epactoidini trib. nov. Grebennikovius is recovered as sister to Epactoides, while Ochicanthon emerges as sister to them both. The disjunct distribution of our focal clade is unusual within the subfamily Scarabaeinae. Bayesian divergence time estimates and ancestral range reconstructions indicate an African origin of the crown group of the tribe Epactoidini trib. nov. in the early mid Eocene, ca. 46 Ma. The divergence between Epactoides and its sister is dated to 32.3 Ma, while the crown age for the genus Ochicanthon is dated to 27 Ma. We investigate the factors that may have shaped the current distribution of the tribe Epactoidini trib. nov. The formation of the Gomphotherium landbridge, along with favourable environmental conditions would have allowed dry-intolerant organisms, such as Ochicanthon, to disperse out of Africa. Remarkable climatic stability of the Eastern Arc Mountains was critical for the retention of the monotypic genus Grebennikovius. We suggest two subsequent overwater dispersal events: the migration of the most recent common ancestor (MRCA) of Epactoides from Africa to Madagascar (32.3-29.5 Ma); the lately dispersal of the MRCA of the today's extinct Epactoides giganteus Rossini, Vaz-de-Mello & Montreuil to Réunion island from Madagascar (3.4 Ma). We suggest that the high potential of dispersal of Epactoidini trib. nov. dung beetles and the strict association to forest habitat might have triggered two major radiations, one in Madagascar and one in the Oriental Region.
... On the other hand, the boreotropical and Gomphotherium dispersal scenarios assume younger lineage age and suggest the pivotal role of forest corridors in driving biotic exchange between Africa and Asia. For example, out-of-Africa migrations via the Gomphotherium corridor have been well documented for tetrapods (Harzhauser et al., 2007) and snakes (Pook et al., 2009), while Asia-to-Africa dispersals through the same corridor have been proposed for termites (Bourguignon et al., 2017), butterflies (Kaliszewska et al., 2015;Toussaint et al., 2019Toussaint et al., , 2021, amphibians (Yuan et al., 2018) and lizards (Tamar et al., 2016(Tamar et al., , 2018. However, it is still unclear whether these four scenarios can sufficiently explain all cases of disjunct Paleotropical distributions. ...
... (Morley, 2007;Pound et al., 2012). The existence of this corridor is used to explain the migrations of tropical biotas between Africa and Asia in both directions (Bourguignon et al., 2017;Cruaud et al., 2011;Toussaint et al., 2019Toussaint et al., , 2021Zhou et al., 2012). The Gomphotherium corridor likely existed between 27 and 14 Ma but these dates are still debated (Hamon et al., 2013;Pirouz et al., 2017;Rögl, 1999 ...
Article
Full-text available
Paleotropical clades with largely disjunct distributions are ideal models for biogeographic reconstructions. The dung beetle genera Grebennikovius Mlambo, Scholtz & Deschodt, Epactoides Olsouffief and Ochicanthon Vaz‐de‐Mello are distributed in Tanzania, Madagascar and Réunion, and the Oriental region, respectively. We combine morphology and molecular dataset to reconstruct the phylogenetic relationships between these taxa. Our analyses corroborate previous hypotheses of monophyly of the group, which is here described as new tribe Epactoidini trib. nov. Grebennikovius is recovered as sister to Epactoides, while Ochicanthon emerges as sister to them both. The disjunct distribution of our focal clade is unusual within the subfamily Scarabaeinae. Bayesian divergence time estimates and ancestral range reconstructions indicate an African origin of the crown group of the tribe Epactoidini trib. nov. in the early mid Eocene, ca. 46 Ma. The divergence between Epactoides and its sister is dated to 32.3 Ma, while the crown age for the genus Ochicanthon is dated to 27 Ma. We investigate the factors that may have shaped the current distribution of the tribe Epactoidini trib. nov. The formation of the Gomphotherium landbridge, along with favourable environmental conditions would have allowed dry‐intolerant organisms, such as Ochicanthon, to disperse out of Africa. Remarkable climatic stability of the Eastern Arc Mountains was critical for the retention of the monotypic genus Grebennikovius. We suggest two subsequent overwater dispersal events: the migration of the most recent common ancestor (MRCA) of Epactoides from Africa to Madagascar (32.3–29.5 Ma); the lately dispersal of the MRCA of the today's extinct Epactoides giganteus Rossini, Vaz‐de‐Mello & Montreuil to Réunion island from Madagascar (3.4 Ma). We suggest that the high potential of dispersal of Epactoidini trib. nov. dung beetles and the strict association to forest habitat might have triggered two major radiations, one in Madagascar and one in the Oriental Region. This study corroborates the monophyly of the dung beetle clade Grebennikovius + Epactoides + Ochicanthon, which is described as a new tribe Epactoidini trib. nov. Biogeographic reconstructions indicate an African origin for Epactoidini (ca 46 Ma). Ochicanthon would have dispersed to Asia through the Gomphotherium landbridge (ca 46–27 Ma). Eastern Arc Mountains played as retention area for Grebennikovius, while Epactoides would have reached Madagascar (32.3–29.5 Ma) and Réunion island (3.4 Ma) through two overwater dispersal events.
... Reconstruction of ancestral states. We reconstructed the ancestral states of 33 characters (see Table S1) for 21 species using a phylogenetic tree of termites inferred from full mitochondrial genomes 82,109 . Alarm characters were selected from our observations and existing literature, ecological characters were selected according to our estimation of possible importance. ...
Article
Full-text available
Termites (Blattodea: Isoptera) have evolved specialized defensive strategies for colony protection. Alarm communication enables workers to escape threats while soldiers are recruited to the source of disturbance. Here, we study the vibroacoustic and chemical alarm communication in the wood roach Cryptocercus and in 20 termite species including seven of the nine termite families, all life-types, and all feeding and nesting habits. Our multidisciplinary approach shows that vibratory alarm signals represent an ethological synapomorphy of termites and Cryptocercus. In contrast, chemical alarms have evolved independently in several cockroach groups and at least twice in termites. Vibroacoustic alarm signaling patterns are the most complex in Neoisoptera, in which they are often combined with chemical signals. The alarm characters correlate to phylogenetic position, food type and hardness, foraging area size, and nesting habits. Overall, species of Neoisoptera have developed the most sophisticated communication system amongst termites, potentially contributing to their ecological success. The vibroacoustic and chemical alarm communication in the wood roach Cryptocercus and in 20 termite species are studied to reveal that the Neoisoptera species have developed the most sophisticated communication system, which could contribute towards their ecological success.
Article
Full-text available
Little is known about the phylogeography of termites in the Neotropical region. Here, we explored the genetic patterns and phylogeographical processes in the evolutionary history of Nasutitermes kemneri, an endemic termite of the South American diagonal of open formations (DOF) formed by the Chaco, Cerrado, and Caatinga phytogeographic domains. We sampled 60 individuals across the three domains of the DOF, and using the mitochondrial genes 16S, COI, and COII, as well as the nuclear gene ITS, evaluated the genetic diversity and divergence time of the populations, along with their genetic structure. The results show a strong genetic and spatial structure within the samples, evidencing the existence of two well-differentiated genetic groups: the Northeastern and the Southwestern populations, which diverged about 2.5 Mya, during the Pliocene-Pleistocene boundary. The Northeastern population, which encompasses Caatinga and northern portions of Cerrado, has an intricate structure and seems to have suffered repetitive retraction-expansion events due to climactic fluctuations during the Quaternary. The Southwestern population, which ranges from central-south Cerrado to the northeast peripherical portions of the Chaco, displays a star-shaped haplotype structure, indicating that this region may have acted as a refugia during interglacial periods.
Article
The complete mitochondrial genome of Cryptotermes domesticus (Haviland) was sequenced and annotated to study its characteristics and the phylogenetic relationship of C. domesticus to other termite species. The mitogenome of C. domesticus is a circular, close, and double-stranded molecule with a length of 15,655 bp. The sequenced mitogenome contains 37 typical genes, which are highly conserved in gene size, organization, and codon usage. Transfer RNA genes (tRNAs) also have typical secondary structures. All of the 13 protein-coding genes (PCGs) start with an ATN codon, except for nad4, which starts with GTG and terminates with the terminal codon TAA and TAG or the incomplete form T-- (cox2 and nad5). Most tRNAs have a typical cloverleaf structure, except for trnS1, in which this form is replaced by a simple loop and lacks the dihydrouridine (DHU) arm. The nucleotide diversity (Pi) and nonsynonymous (Ka)/synonymous (Ks) mutation rate ratios indicate that nad1, cox1, and cox3 are the most conserved genes, and that cox1 has the lowest rate of evolution. In addition, an 89 bp repeated sequence was found in the A + T-rich region. Phylogenetic analysis was performed using Bayesian inference (BI) and maximum likelihood (ML) methods based on 13 PCGs, and the monophyly of Kalotermitidae was supported. Research highlights • We sequence and analyze the complete mitochondrial genome of Cryptotermes domesticus. • We analyze the genome size and nucleotide composition; codon usage, gene overlaps, and intergenic spacers; tRNA secondary structure, and the A + T-rich region. • The phylogenetic relationship of Cryptotermes domesticus among Kalotermitidae is clarified.
Article
Full-text available
Past evolutionary adaptations to Australia's aridification can help us to understand potential responses of species in the face of global climate change. Here, we focus on the Australian‐endemic genus Drepanotermes, also known as Australian harvester termites, which are mainly found in semi‐arid and arid regions of Australia. We used species delineation, phylogenetic inference, and ancestral state reconstruction to investigate the evolution of mound‐building in Drepanotermes and in relation to reconstructed past climatic conditions. Our findings suggest that mound‐building evolved several times independently in Drepanotermes, apparently facilitating expansions into tropical and mesic regions of Australia. Phylogenetic signal of bioclimatic variables, especially of limiting environmental factors (e.g. precipitation of warmest quarter), suggests that climate exerts a strong selective pressure. Finally, we used environmental niche modeling to predict present and future habitat suitability for eight Drepanotermes species. Abiotic factors such as annual temperature contributed disproportionately to calibrations, while the inclusion of biotic factors like predators and vegetation cover improved ecological niche models in some species. A comparison between present and future habitat suitability under two different emission scenarios revealed continued suitability of current ranges as well as substantial habitat gains for most studied species. Human‐mediated climate change is occuring more quickly than these termites can disperse into newly suitable habitat, however their role in stabilizing arid ecosystems may allow them to mitigate effects on some other organisms at a local level. This article is protected by copyright. All rights reserved
Article
Full-text available
Termites are undoubtedly key soil organisms in tropical and subtropical soils. They are soil engineers in influencing the physical, chemical, and biological properties of soils and, consequently, water dynamics in tropical and subtropical ecosystems. To appreciate the effect of termites on soil, there is a need for a thorough understanding of the ecological needs and building strategies of termites and the mechanisms regulating termite diversity at local and regional scales. Termite impacts on soil properties and water dynamics can be differentiated at four different scales: (i) at the landscape scale, where termites act as heterogeneity drivers; (ii) at the soil profile scale, where termites act as soil bioturbators; (iii) at the aggregate scale, where they act as aggregate reorganizers; (iv) and last, at the clay mineral scale, where they can act as weathering agents. Last, we discuss recent literature on termite engineering published in the last 10 years in the major journals of soil science and suggest new research topics that could contribute to improved knowledge of the impact of termites on soil properties and water dynamics.
Article
Full-text available
Reticulitermes, Heterotermes and Coptotermes form a small termite clade with partly overlapping distributions. Although native species occur across all continents, the factors influencing their distribution are poorly known. Here, we reconstructed the historical biogeography of these termites using mitochondrial genomes of species collected on six continents. Our analyses showed that Reticulitermes split from Heterotermes + Coptotermes at 59.5 Ma (49.9–69.5 Ma 95% CI), yet the oldest split within Reticulitermes (Eurasia and North America) is 16.1 Ma (13.4–19.5 Ma) and the oldest split within Heterotermes + Coptotermes is 36.0 Ma (33.9–40.5 Ma). We detected 14 disjunctions between biogeographical realms, all of which occurred within the last 34 Ma, not only after the break-up of Pangaea, but also with the continents in similar to current positions. Land dispersal over land bridges explained four disjunctions, oceanic dispersal by wood rafting explained eight disjunctions, and human introduction was the source of two recent disjunctions. These wood-eating termites, therefore, appear to have acquired their modern worldwide distribution through multiple dispersal processes, with oceanic dispersal and human introduction favoured by the ecological traits of nesting in wood and producing replacement reproductives. © 2016 The Author(s) Published by the Royal Society. All rights reserved.
Chapter
Full-text available
Many mammals, ranging from antelope to elephant shrews, eat ants and termites. The specialized mammalian myrmecophages (ant- and termite-eaters) such as aardvarks and pangolins have long drawn attention, but little work has been done on general predator-prey relationships between mammals and ants and termites.
Book
The book is a new compendium in which leading termite scientists review the advances of the last 30 years in our understanding of phylogeny, fossil records, relationships with cockroaches, social evolution, nesting, behaviour, mutualisms with archaea, protists, bacteria and fungi, nutrition, energy metabolism,population and community ecology, soil conditioning, greenhouse gas production and pest status.
Article
We investigate a neutral model for speciation and extinction, the constant rate birth-death process. The process is conditioned to have $n$ extant species today, we look at the tree distribution of the reconstructed trees-- i.e. the trees without the extinct species. Whereas the tree shape distribution is well-known and actually the same as under the pure birth process, no analytic results for the speciation times were known. We provide the distribution for the speciation times and calculate the expectations analytically. This characterizes the reconstructed trees completely. We will show how the results can be used to date phylogenies.
Article
Odontotermes formosanus is the most serious termite pest species of dams and dikes in Southern China. The dispersal distances of the alates are important to better understand its impact and to determine the effectiveness of control tactics. A mark-recapture study using fluorescent spray paints was conducted to characterize dispersal distances of an O. formosanus colony which was located in the Longdong reservoir dam, Guangzhou, China. O. formosanus alates were capable of flying 120 to at least 743 m in the direction of the low prevailing wind. These results could help to formulate a management strategy against O. formosanus. The advantages of the fluorescent spray paint/fluorescence microscopy technique is also discussed.
Article
The most diverse and best-preserved paleofauna of the higher termites heretofore known, all found in Miocene amber of the Dominican Republic, is described. The imago of Coptotermes priscus Emerson is redescribed, and the soldier of C. priscus, the first known fossil soldier of this genus, is described. The fauna includes the following 29 new species, all in existing genera, with Krishna and Grimaldi as authors of each: in the Rhinotermitidae, two new species based on imagoes of each-Coptotermes hirsutus and C. paleodominicanus; in the Termitidae, 23 new species based on imagoes-Amitermes lucidus, Anoplotermes bohio, A. cacique, A. carib, A. maboya, A. naboria, A. nitaino, A. quisqueya, A. taino, Atlantitermes antillea, A. caribea, A. magnoculus, Microcerotermes insulanus, M. setosus, Nasutitermes amplioculatus, N. incisus, N. magnocellus, N. medioculatus, N. pilosus, N. seminudus, Subulitermes hispaniola, S. insularis, and Termes primitivus; in the Nasutitermitinae four new species based on nasute soldiers-Caribitermes hispaniola, Nasutitermes rotundicephalus, Parvitermes longinasus, and Velocitermes bulbus. This brings the total termite fauna in Dominican amber to four families, 17 genera, and 39 species, a number that exceeds that of the present-day fauna of Hispaniola. Biogeographical, paleoecological, and phylogenetic implications of the Dominican amber termites are discussed.