*For correspondence:
joep@caltech.edu
Competing interests:
The
authors declare that no
competing interests exist.
Funding:
See page 11
Received:
09 January 2019
Accepted:
11 March 2019
Published:
16 April 2019
Reviewing editor:
John A Long,
Flinders University, Australia
Copyright Zhou et al. This
article is distributed under the
terms of the
Creative Commons
Attribution License,
which
permits unrestricted use and
redistribution provided that the
original author and source are
credited.
A Mesozoic clown beetle myrmecophile
(Coleoptera: Histeridae)
Yu-Lingzi Zhou
1,2
, Adam S
́
lipin
́
ski
2
, Dong Ren
3
, Joseph Parker
4
*
1
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology,
Chinese Academy of Sciences, Beijing, China;
2
Australian National Insect Collection,
CSIRO, Canberra, Australia;
3
College of Life Sciences, Capital Normal University,
Beijing, China;
4
Division of Biology and Biological Engineering, California Institute of
Technology, Pasadena, United States
Abstract
Complex interspecies relationships are widespread among metazoans, but the
evolutionary history of these lifestyles is poorly understood. We describe a fossil beetle in 99-
million-year-old Burmese amber that we infer to have been a social impostor of the earliest-known
ant colonies.
Promyrmister kistneri
gen. et sp. nov. belongs to the haeteriine clown beetles
(Coleoptera: Histeridae), a major clade of ‘myrmecophiles’—specialized nest intruders with
dramatic anatomical, chemical and behavioral adaptations for colony infiltration.
Promyrmister
reveals that myrmecophiles evolved close to the emergence of ant eusociality, in colonies of stem-
group ants that predominate Burmese amber, or with cryptic crown-group ants that remain largely
unknown at this time. The clown beetle-ant relationship has been maintained ever since by the
beetles host-switching to numerous modern ant genera, ultimately diversifying into one of the
largest radiations of symbiotic animals. We infer that obligate behavioral symbioses can evolve
relatively rapidly, and be sustained over deep time.
DOI: https://doi.org/10.7554/eLife.44985.001
Introduction
A pervasive feature of colony-forming insect societies is the profusion of intruder arthropods that
have evolved to exploit their rich resources (
Kistner, 1979
;
Kistner, 1982
;
Ho
̈
lldobler and Wilson,
1990
;
Parker, 2016
). The diversity of such organisms is impressive, with
~
10,000 species hypothe-
sized to target or profit from ant nests alone (
Elmes, 1996
). Hostility of ant workers to virtually all
non-nestmate organisms has selected for defensive or host-deceptive adaptations in myrmecophiles
which are often phenotypically remarkable, involving changes in anatomy, chemical ecology and
behavior (
Kistner, 1979
;
Kistner, 1982
;
Ho
̈
lldobler and Wilson, 1990
;
Parker, 2016
). In a number
of cases, traits have arisen that enable the myrmecophile to manipulate worker behavior, circumvent-
ing aggression and enabling social interactions to evolve that assimilate the symbiont into colony
life. Such relationships rank among the most behaviorally intimate interactions known between ani-
mal species (
Kistner, 1979
;
Ho
̈
lldobler and Wilson, 1990
;
Parker, 2016
), and are typically achieved
by the myrmecophile’s capacity to mimic the chemical and/or tactile cues involved in nestmate rec-
ognition (
Kistner, 1979
;
Ho
̈
lldobler and Wilson, 1990
;
Parker, 2016
). The clown beetle family His-
teridae includes multiple lineages that have independently evolved myrmecophily (
Parker, 2016
;
Kovarik and Caterino, 2005
), including Haeteriinae, a subfamily of
~
335 described species compris-
ing possibly the single largest radiation of myrmecophiles known within the Coleoptera
(
Parker, 2016
;
Kovarik and Caterino, 2005
;
Helava et al., 1985
). We report the discovery of a
crown-group haeteriine in Upper Cretaceous Burmese amber, revealing that the clown beetle-ant
interaction has an exceptionally deep evolutionary history. To our knowledge, the relationship con-
stitutes the most ancient behavioral symbiosis known in the Metazoa.
Zhou
et al
. eLife 2019;8:e44985.
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RESEARCH ARTICLE
Results and discussion
Systematic palaeontology
Order Coleoptera Linnaeus, 1758
Superfamily Histeroidea Gyllenhal, 1808
Family Histeridae Gyllenhal, 1808
Subfamily Haeteriinae Marseul, 1857
Promyrmister kistneri
Zhou, S
́
lipin
́
ski and Parker gen. et sp. nov.
Holotype
Sex unknown. CNU-008021, deposited in Key Laboratory of Insect Evolution and Environmental
Changes, Capital Normal University, Beijing. The holotype is well preserved in a small, transparent
amber piece, 5.5 mm length
3.5 mm width (
Figure 1—figure supplement 1A
). The entire external
anatomy is observable (
Figure 1A
--
C
), but the left region of the dorsal side is partially covered by
white exudate (
Figure 1A,G
) emanating from the ventral side of the pronotal margin (arrow in
Figure 1A,G
).
Diagnosis of new genus and species
Haeteriine histerid that is distinguished from all other genera and species of Haeteriinae by posses-
sion of the following combination of characters: (1) deep depression behind meso- and metacoxae
(
Figure 1C,H
); (2) metaventral postcoxal line recurved and extending laterally to metanepisternum
(
Figure 1B,C
; (3) three complete striae on each elytron (
Figure 1A
); (4) lack of dorsal furrows on pro-
notum demarcating glandular lobe (
Figure 1A,B
); (5) strongly developed apical spur on protibia
eLife digest
Many animals live lives that are closely intertwined with those of other species.
While a clown fish sheltering within the tentacles of a sea anemone may be a textbook example,
‘symbiotic’ interactions that occur inside ant nests are among some of the most dramatic.
Known as myrmecophiles – after the Greek for ‘ant lovers’, many insects, spiders and mites have
evolved to live alongside ants in one way or another. Some of these animals display elaborate
behaviors – like mouth-to-mouth feeding or grooming of worker ants – which assimilates them into
the nest society; some even release chemicals that mimic the ants’ own scents to avoid being
detected as an intruder.
The earliest examples of ancestral ants are found encapsulated in 99-million-year-old amber from
a mine in northern Myanmar (Burma). Zhou et al. have now discovered an ancient beetle, perfectly
preserved in the same amber deposits, that may have also lived within the colonies of those earliest-
known ants. Based on its appearance, the beetle – named
Promyrmister kistneri
– belongs within a
subfamily of clown beetles (called the Haeteriinae) that are all specialized nest intruders with
dramatic behavioral and chemical adaptations that help them to infiltrate ant colonies.
The ancient clown beetle shares several of features with its modern relatives – including thick,
spiked legs and well-protected head and antennae – which are believed to help the beetles
withstand handling by the ants’ jaws. The specimen also has glands near the base of its legs,
implying that it also released chemical signals that may have helped it to deceive or pacify the
ancient ants.
The fact that this extinct clown beetle is as old as the earliest-known ants implies that the close
relationship between these insects has been sustained for an exceptionally long time. It is potentially
the oldest known example of a symbiotic interaction in the animal kingdom that depends on social
interactions between the two organisms. However, the host ants of
Promyrmister
are believed to be
long-extinct, suggesting that symbiotic clown beetles had to switch to living inside colonies of
modern ants to circumvent their own extinction. This flexibility to adapt to new partner species may
be a critical feature that allows some symbiotic organisms to persist throughout evolution.
DOI: https://doi.org/10.7554/eLife.44985.002
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et al
. eLife 2019;8:e44985.
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Figure 1.
Promyrmister kistneri
gen.et sp. nov. (
A
) Dorsal habitus of holotype CNU-008021 with origin of exudate globule (black arrow) and elytral striae
(white arrows) indicated; the three lateral striae are complete (top three arrows), the three medial striae appear incomplete. (
B
) Right lateral habitus with
flight wing indicated. (
C
) Ventral habitus, boxed region expanded in panel H. (
D
) Head, dorsal and (inset) frontal views, with antennal scapes and
frontoclypeal carina (FC) indicated. (
E
) Right foreleg, laterally expanded femur and tibia indicated. (
F
) Proventral-mesoventral boundary showing
proventral keel with posterior incision. (
G
) Left pronotal margin, lateral view, showing possible origin of putative glandular exudate; arrow in G
corresponds to that in panel A. (
H
) Ventrite one showing proximal leg segments (Trc: trochanter) and postcoxal gland openings (white arrows), with
globule of putative exudate emanating from left postcoxal gland opening.
DOI: https://doi.org/10.7554/eLife.44985.003
The following figure supplements are available for figure 1:
Figure supplement 1.
Amber piece and frontal view of holotype of Promyrmister kistneri sp.nov.
Figure 1 continued on next page
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et al
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(
Figure 1D,E
); (6) frontoclypeus carinate medially (
Figure 1D
,
Figure 1—figure supplement 1B,C
);
(7) triangular-shaped cavities to receive scapes of antennae (
Figure 1—figure supplement 1B,C
); (8)
glandular opening in postcoxal cavity behind metacoxae (
Figure 1H
;
Figure 1—figure supplement
2A,B,D
).
Promyrmister
specifically differs from the closely related
Haeterius
in having deep episto-
mal depressions (
Figure 1—figure supplement 1B,C
; compare to
Figure 2—figure supplement
1D
), carinated epistomal striae convergent in the middle (
Figure 1—figure supplement 1B,C
) and
paddle-shaped protibia with large apical spur (
Figure 1D,E
).
Locality and age
The holotype inclusion is derived from an amber mine located near Noije Bum, Tanaing, Kachin,
Myanmar. The U-Pb dating of zircons from the volcanoclastic matrix yielded an age of 98.79
±
0.62
million years (
Shi et al., 2012
).
Etymology
The generic name
Promyrmister
is a combination of the Greek
p
%
o
(pro) meaning ‘before’ or ‘early’,
u
ˆ
h
(myrmex) meaning ‘ant’, and
Hister
Linnaeus, type genus of Histeridae. The name refers to
the likely symbiotic habits of the fossil taxon inside early ant colonies. The gender is masculine. The
specific epithet recognizes the lifetime contribution of Dr. David H. Kistner, a global authority on
social insect symbionts.
Description
Length 3.2 mm, width 2.3 mm. Body elongate oval (
Figure 1A,C
), moderately convex (
Figure 1B
);
black or dark brown with dorsal surfaces bearing short and somewhat squamiform setae, visible
along pronotal and elytral edges but on dorsal side often obscured by accumulation of water/dirt
and appearing as tiny granules; interstices between setae moderately to distinctly shiny.
Head only partially visible, deeply inserted into prothorax (
Figure 1D
;
Figure 1—figure supple-
ment 1B
). Frons with distinct frontoclypeal carina (FC in
Figure 1D
), and widely interrupted frontal
stria, the lateral parts of which extend to the frontoclypeal carina, connecting to inwardly-arching
epistomal striae (
Figure 1—figure supplement 1C
). Clypeus bordered by deep epistomal depres-
sions to receive antennal scapes in repose (
Figure 1—figure supplement 1B
). Clypeus and labrum
apparently fused but with distinct transverse ridge above the base of labrum. Mandibles strongly
arcuate apically. Antennal scape large and triangular (
Figure 1—figure supplement 1B
), covering
eye, and densely rugose dorsally.
Prothorax (length 1.0 mm and width 1.8 mm) widest at base, sides weakly rounded, converging
anteriorly, anterior angles distinctly projecting and rounded; posterior angles weakly obtuse
(
Figure 1A
). Lateral margins crenulate, each projection bearing weakly squamiform setae. Pronotum
with marginal stria complete anteriorly and along lateral margins; sides without impressions or obvi-
ous gland openings along lateral carina; disc weakly convex, setose. Proventral lobe strongly promi-
nent medially, covering most of ventral head surface and extending laterally to antennal cavities
without visible marginal stria. Prosternal process (proventrite) narrowly elevated with apex about 0.1
times as broad as prothorax, expanding apically and deeply emarginate at apex (
Figure 1F
); proster-
nal carinae converging anteriorly but not apparently joined; junction between proventrite and pros-
ternal lobe deeply depressed. Antennal cavity present on anterior angles of hypomeron, deep and
completely closed from below via proventral alae (
Figure 1—figure supplement 1B
). Procoxae not
clearly visible. Trochanter large, triangular and bearing several long setae; profemur very broad,
width nearly 0.45 mm, and flat, covering most of the ventral side of prothorax (
Figure 1E
); protibia
flat and expanded, width about 0.38 mm, bearing row of strong spines along external edge and an
apical spur (
Figure 1E
); protarsi short and thin, sitting in straight groove on dorsal side of protibia
(
Figure 1D
). Scutellum obscured dorsally by secretion (
Figure 1A
). Elytra (1.8 mm length
2.3 mm
Figure 1 continued
DOI: https://doi.org/10.7554/eLife.44985.004
Figure supplement 2.
Further morphology of
Promyrmister
.
DOI: https://doi.org/10.7554/eLife.44985.005
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width), with relatively complete dorsal striae 1
--
three and reduced striae 4–6 (white arrows in
Figure 1A
); outer subhumeral stria complete, sutural stria very fine and visible apically.
Mesoventrite between mesocoxae very broad, about 1/3 of body width at the same position
(
Figure 1C
); anterior margin projecting medially fitting into prosternal process (
Figure 1F
); Margin
between metaventrite and visible abdominal ventrite one shallowly grooved. Ventrite one weakly
convex medially, deeply concave laterally (
Figure 1C
) to accommodate strongly flattened legs. Post-
coxal lines behind meso- and metacoxae completely recurved dorsally; discrimen complete. Hind
coxae triangular (
Figure 1C,H
;
Figure 1—figure supplement 2A–C
), large and broadly separated
from each other, with numerous regular rows of oblique striae on inner surface (
Figure 1—figure
supplement 2A–C
); hind femur oval-shaped, distinctly large and flat, enveloping small and setose
trochanter (
Figure 1C,H
). Hind tibia flat, paddle-like, about as broad as femur (
Figure 1C
), with a
row of strong spines along external edge, double rows of stiff and apically modified setae along
inner edge, inner surface with transverse ridges and row of pointed spines before; apical spur small.
Tarsal formula 5-5-5. Hind tarsi slim, locating on inner side of tibia, tarsomere one longest, length
subequal to tarsomeres 2
--
four combined. Wings visible apically (
Figure 1B
), presumed functional.
Abdomen with median part of ventrite one delimited to a flat and polished central plate by inner
abdominal stria, much longer than the remaining ventrites combined (
Figure 1C
); postcoxal line
(outer abdominal stria) recurved and strongly diverging laterally (
Figure 1B,C
); also with deeply
depressed rest for hind tibia outside the postcoxal line. Large abdominal gland opening behind hind
coxa located between inner and outer abdominal striae (
Figure 1H
), on right side with exudate flow-
ing out (paired arrows in
Figure 1H
;
Figure 1—figure supplement 2B,D
, note that laser reflectance
indicates this is solidified material and not a gas/air bubble, which would appear dark). Ventrites
2
--
four equal in length, without posterior marginal striae.
Systematic position
The fossil beetle is placed in Histeridae based on its possession of the following characters
(
Kovarik and Caterino, 2000
): (i) a broad and compact body shape (
Figure 1A,C
); (ii) striate elytra
that expose the two posterior abdominal tergites (
Figure 1A
); ii) five visible abdominal sternites
(
Figure 1C
); (iv) short legs with broad, flattened tibiae (
Figure 1C,E
); (v) antenna short and genicu-
late with compact, 3-segmented club (
Figure 1—figure supplement 1B
); (vi) antenna retracting into
cavity underneath the pronotum (
Figure 1—figure supplement 1B
); (vii) tarsal formula 5-5-5. Of the
11 histerid subfamilies (
Bouchard et al., 2011
),
Promyrmister
can be placed unequivocally in the
subfamily Haeteriinae based on the following characters: head deflexed, with clypeus arched down-
wards in a different plane to the vertex (
Figure 1D
); antenna with enlarged, triangular scape
received in repose in frontal groove and hiding the eye (
Figure 1D
;
Figure 1—figure supplement
1B,C
); antennal cavities located on hypomeron (
Figure 1—figure supplement 1B
), covered from
below by proventral alae; proventral lobe strongly developed anteriorly, covering head from below,
and extending laterally to form proventral alae (without lateral notch); proventral keel narrowly ele-
vated between coxae and distinctly emarginate posteriorly to receive the projecting mesoventral
process (
Figure 1F
). Additionally, the front, mid, and hind legs are extremely broad (
Figure 1C,E
),
which is a feature of the clade
Yarmister
+ Haeteriinae (
Caterino and Tishechkin, 2015
), in which
Yarmister
lacks the distinctly elevated proventral keel with posterior incision, which is present in
Pro-
myrmister
and is an autapomorphy of the Haetaeriinae (
Helava et al., 1985
). The labrum of the fossil
specimen may also be fused, but fossilization position precludes definitive assessment.
Within Haeteriinae, the new taxon appears to bear a close relationship to the genus
Haeterius
Erichson and some closely allied genera that share several morphological characters supporting their
monophyly (
Ye
́
lamos, 1997
), principally the broad and externally rounded tibiae, the deep depres-
sions behind meso- and metacoxae to accommodate retracted legs (
Figure 1C,H
) (
Caterino and
Tishechkin, 2015
), the metaventral postcoxal line being recurved and extending laterally to the
metanepisternum (
Figure 1B,C
), and the presence of three complete striae on each elytron
(
Figure 1A
). Morphological features of the extant
Haeterius
, with key character states shared with
Promyrmister
, are shown in
Figure 2—figure supplement 1
(see Diagnosis for separation of
Pro-
myrmister
and
Haeterius
). Consistent with our evaluation of
Promyrmister
’s likely phylogenetic place-
ment, both cladistic and Bayesian analysis of a set of morphological characters (
Caterino and
Tishechkin, 2015
) from the fossil specimen and a selection of Recent histerid taxa places the new
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taxon within Haeteriinae as sister to
Haeterius
(
Figure 2A,B
;
Figure 2—figure supplements 2
and
3
). We infer that
Promyrmister
represents an extinct Cretaceous lineage that belongs within the
crown-group of Haeteriinae.
Promyrmister
and deep-time persistence of a social symbiosis
Symbiotic relationships in which different animal species interact socially with each other have arisen
sporadically across the metazoan tree of life. Such relationships encompass a spectrum of depen-
dency, from transient, facultative associations seen in mixed-species groups of insectivorous birds
(
Sridhar et al., 2009
), cetaceans and ungulates (
Stensland et al., 2003
;
Goodale et al., 2017
), to
obligate symbiotic lifestyles typified by brood parasitic cuckoos, cowbirds (
Johnsgard, 1997
), mutu-
alistic cleaner fish (
Grutter, 1999
) and oxpeckers (
Nunn et al., 2011
). Of all animal groups, however,
the complex societies of ants play host to the greatest diversity of behavioral symbionts. Several
major radiations of myrmecophiles are known, each containing hundreds of symbiotic species,
including the lycaenid butterflies (
Pierce et al., 2002
), eucharitid wasps (
Murray et al., 2013
), paus-
sine ground beetles (
Moore and Robertson, 2014
) and multiple lineages of rove beetles (
Kist-
ner, 1979
;
Kistner, 1982
;
Parker, 2016
;
Parker and Grimaldi, 2014
;
Seevers, 1965
;
Maruyama and Parker, 2017
). The diversity and often-broad geographic ranges of these clades
imply that their relationships with ants are evolutionarily ancient (
Parker and Grimaldi, 2014
;
Yamamoto et al., 2016
). Although fossil myrmecophiles are known from as far back as the Eocene
(
Parker and Grimaldi, 2014
;
Wasmann, 1929
), ant eusociality is known to be at least twice as old,
Figure 2.
Phylogenetic relationships of
Promyrmister
. (
A
) Consensus Bayesian Inference (BI) tree of representative histerid taxa including Haeteriinae,
and
Promyrmister
. Posterior probabilities above 0.8 are shown on branches. (
B
) The consensus parsimony tree (MP) using TNT under the Traditional
Search; bootstrap percentages above 80 are shown on branches. (
C
) Habitus photograph of
Haeterius
(
H. ferrugineus
), an inferred extant close relative
of
Promyrmister
(photo credit: C. Fa
̈
gerstro
̈
m) (
D, E
) Living
Haeterius ferrugineus
beetles interacting with
Formica
(
D
) and
Lasius
(
E
) host ants (photo
credit: P. Kra
́
sensky
́
). (
F
) Reconstruction of
Promyrmister
with stem-group host ant and larva (ant based on
Gerontoformica
).
DOI: https://doi.org/10.7554/eLife.44985.006
The following figure supplements are available for figure 2:
Figure supplement 1.
Scanning electron micrographs of extant
Haeterius ferrugineus
(Olivier, 1789).
DOI: https://doi.org/10.7554/eLife.44985.007
Figure supplement 2.
Part A of single tree obtained by parsimony analysis of morphological matrix using implied weighting (K = 13) in TNT.
DOI: https://doi.org/10.7554/eLife.44985.008
Figure supplement 3.
Part B of single tree obtained by parsimony analysis of morphological matrix using implied weighting (K = 13) in TNT.
DOI: https://doi.org/10.7554/eLife.44985.009
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. eLife 2019;8:e44985.
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with the earliest definitively social ants occurring in Upper Cretaceous Burmese amber (
Barden and
Grimaldi, 2016
). Whether their colonies were targeted by myrmecophiles has, however, been
unclear: ants are comparatively scarce in Cretaceous ambers (
Grimaldi and Agosti, 2000
;
LaPolla et al., 2013
;
Barden, 2016
;
Barden, 2018
), and myrmecophilous invertebrates typically live
at densities orders of magnitude lower than their hosts (
Kistner, 1979
). The unlikely discovery of a
myrmecophile clown beetle in Burmese amber reveals that a major radiation of ant symbionts has its
origins in Mesozoic ant societies.
Analysis of
Promyrmister’
s morphology and phylogenetic position indicates the new genus repre-
sents an extinct lineage within the crown-group of Haeteriinae, a clade of obligate myrmecophiles
(
Figure 2A,B
;
Figure 2—figure supplements 2
and
3
; see Materials and methods). In haeteriine
taxa for which detailed behavioral observations exist, the beetles have been shown to engage in inti-
mate behaviors with ants, involving stomodeal trophallaxis (mouth-to-mouth feeding)
(
Wheeler, 1908
;
Henderson and Jeanne, 1990
;
Akre, 1968
), grooming workers with their appen-
dages (and being groomed or licked by hosts in return) (
Akre, 1968
), physically grasping onto ants
(phoresis) (
Akre, 1968
;
von Beeren and Tishechkin, 2017
), or being carried around nests by work-
ers (
Kistner, 1982
). Mimicry of colony cuticular hydrocarbons occurs (
Lenoir et al., 2012
), as well as
chemical manipulation of host ants via ‘appeasement’ substances exuded from gland openings on
the margins of the prothorax (
Kistner, 1982
;
Seyfried, 1928
) or in the postcoxal regions of the bee-
tle’s underside (
Figure 2—figure supplement 1C
).
Promyrmister
appears to be closely allied to the
extant genus
Haeterius
(
Figure 2A–C
;
Figure 2—figure supplement 1
). This genus and a handful of
closely related taxa including
Eretmotus
,
Sternocoelis
and
Satrapes
comprise the only group of Hae-
teriinae known to occur in the Palaearctic, consistent with the Eurasian palaeolocality of
Promyrmis-
ter
in Burmese amber. Like all of these genera,
Promyrmister
exhibits classical haeteriine attributes
that are thought to be true adaptations for myrmecophily, including broad expansions of the tibiae
with spines on the outer margin (
Figure 2C
;
Figure 2—figure supplement 1E
), short tarsi received
on the outer face of each tibia (
Figure 2—figure supplement 1E
), a triangular antennal scape (
Fig-
ure 2—figure supplement 1D
), pronounced antennal cavities on the prothoracic hypomeron (
Fig-
ure 2—figure supplement 1D
) and a broad proventral lobe to fully embrace the retracted head
(
Figure 2—figure supplement 1B–D
). Those features are thought to be protective modifications
that enable myrmecophile beetles to withstand handling by ant mandibles (
Parker, 2016
).
We and others have previously described rove beetles (Staphylinidae) in the Burmese palaeo-
fauna that were putative symbionts of termite colonies (
Yamamoto et al., 2016
;
Cai et al., 2017
).
These specimens exhibit a defensive ecomorphology and are thought to have been persecuted
intruders that were not behaviorally integrated into their host’s societies (
Yamamoto et al., 2016
;
Cai et al., 2017
). In contrast, Haeteriinae embody a form of true behavioral symbiosis, where the
relationship with host ants can involve social interactions (
Figure 2D,E
; Figure 4). The prothoracic
glandular openings of Haeteriinae that secrete putative appeasement compounds are challenging to
demonstrate even in extant taxa, but in the
Promyrmister
holotype, a large globule of possible exu-
date originates from the left margin of the prothorax, consistent with the position of such glands
(
Figure 1A,G
). Additionally,
Promyrmister
possesses clear postcoxal secretory glands (
Figure 1H
;
Figure 1—figure supplement 2A,B,D
), with a globule of possible exudate emanating from the post-
coxal gland opening on the right side of the body (
Figure 1H
;
Figure 1—figure supplement 2B,D
).
Beyond
Promyrmister
’s phylogenetic position within the Haeteriinae clade, the fossil’s anatomy
implies a chemical strategy to become accepted or at least tolerated inside colonies (hypothetical
reconstruction in
Figure 2F
), akin to modern haeteriine species that have so far been examined
(
Akre, 1968
;
Lenoir et al., 2012
;
Seyfried, 1928
).
What were the Cretaceous host ants of
Promyrmister
? All ants thus far described from Burmese
amber belong to stem-group Formicidae, including members of the extinct subfamily Sphecomyrmi-
nae and three other genera,
Gerontoformica
,
Myanmyrma
and
Camelomecia
that similarly lack
crown-group features but are placed
incertae sedis
within Formicidae (
Barden, 2016
;
Barden, 2018
).
In contrast, fossils of definitive crown-group ant subfamilies are absent, or vanishingly rare, among
the thousands of ant inclusions now recovered from this amber deposit (
Barden, 2016
;
McKellar et al., 2013
) (P. Barden, personal communication). Crown-group ants are also unknown
from contemporaneous Charentese amber (
Barden, 2016
). We posit that the overwhelming preva-
lence of stem-group ants in Burmese amber implies that they were potential hosts of
Promyrmister
(
Figure 2F
). Such a scenario entails that haeteriines may not have originated with the modern ant
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groups that host them today; instead myrmecophily evolved first in stem-group ant colonies, with
the beetles later switching to crown-group ants. We cannot, however, rule out an alternative sce-
nario, that an as-yet undiscovered diversity of crown-group ants were, in fact, present in the Bur-
mese palaeofauna, and it was these that selected for the early evolution of myrmecophily. Molecular
dating indicates that crown-group ants had originated by this time (
Brady et al., 2006
;
Moreau and
Bell, 2013
;
Borowiec et al., 2017a
) (see dotted lines in
Figure 3
). If present in this ancient ecosys-
tem, perhaps their cryptic biologies limited their entrapment in amber.
Whether haeteriines evolved in stem- or crown-group ant colonies, their original hosts are pre-
sumably long-extinct. The present-day host associations of haeteriines imply that these myrmeco-
philes have host-switched between many modern ant lineages (
Figure 3
). The beetles have been
recorded in colonies of ant species scattered across the subfamilies Dolichoderinae, Dorylinae, For-
micinae, Myrmicinae and Ponerinae (
Helava et al., 1985
;
Tishechkin, 2007
) (
Figure 3
). We suggest
that it is this capacity for host switching that may explain the great longevity of the clown beetle-ant
symbiosis. Through host switching, the clade as a whole has circumvented potential coextinction
with host ant lineages that disappeared from the Cretaceous to the present (
Barden and Grimaldi,
2016
;
Barden, 2016
). Moreover, in some cases, the beetles have radiated dramatically with certain
ant groups: the vast majority of the contemporary species richness of Haeteriinae is found in taxa
that have adapted to colonies of Neotropical army ants (Ecitonini), including at least 30 genera asso-
ciated with
Eciton
army ants alone (
Parker, 2016
;
Helava et al., 1985
;
von Beeren and Tishechkin,
2017
;
Tishechkin, 2007
). Some of these haeteriines have remarkable adaptations for life in colonies
of those nomadic ants (
Figure 4
). Neotropical army ants are thought to have begun diversifying
approximately in the Oligocene (
Brady et al., 2014
;
Borowiec et al., 2017b
), implying that the bulk
of haeteriine cladogenesis occurred within this window too, long after the beetles originated in the
Cretaceous.
Figure 3.
Antiquity of
Promymister
implies pervasive host switching of Haeteriinae from Cretaceous to Recent.
Age of
Promyrmister
is shown (red circle). The inferred window of occurrence of stem-group ants is indicated by
the top orange bar. The ages of crown-group ants as a whole, New World (NW) army ants, and other specific
subfamilies and genera that are known hosts of Haeteriinae are also presented. Orange bars extend back from the
Recent to the age of the earliest-known fossil; dotted lines extend back to molecularly-inferred origins of crown
groups. Molecular dating implies crown-group ants existed at the same time as
Promyrmister
, but stem-group
ants are the only ants so far known in Burmese and other contemporaneous ambers. All modern host ant genera
are inferred to have Cenozoic origins, implying extensive host switching between the inferred Early Cretaceous
origin of Haeteriinae and the present day.
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An ancient association between histerids and ants is further suggested by inquiline-like morphol-
ogy in two other Cretaceous clown beetle fossils (
Caterino et al., 2015
;
Caterino and Maddison,
2018
), although unlike
Promyrmister
, the taxonomic affinities of these specimens are ambiguous
and they are not definitive members of wholly symbiotic lineages. We infer that Haeteriinae was a
relatively diverse clade by at least the beginning of the Upper Cretaceous, and likely originated and
began undergoing basal cladogenesis very soon after the inferred Early Cretaceous emergence of
ant eusociality (
Barden and Grimaldi, 2016
;
Grimaldi and Agosti, 2000
;
Barden, 2016
;
Brady et al., 2006
;
Moreau and Bell, 2013
;
Borowiec et al., 2017a
). A time-calibrated molecular
phylogeny of Haeteriinae may provide a more precise estimate of this temporal window. However,
based on such analyses for other myrmecophile taxa, rapid evolution of specialized symbiotic
Figure 4.
Diversity of modern Haeteriinae associated with Neotropical army ants (Ecitonini). (
A
)
Colonides
beetle
walks in an emigration of
Eciton burchellii
army ants. Note the color mimicry of the host ant (Peru; photo: Taku
Shimada). (
B
)
Euxenister
beetle walking alongside an
Eciton hamatum
army ant worker. The long legs facilitate
grooming ants to obtain the colony odor, as well as clinging to emigrating workers (Peru; photo credit: Takashi
Komatsu). (
C
)
Nymphister kronaueri
beetle phoretically attached to the petiole of an
Eciton mexicanum
army ant
worker. The beetles bite onto this part of the ant’s body, enabling them to migrate with the host. The beetle
resembles the ant’s gaster from above, potentially camouflaging the beetles to avoid predation (Costa Rica; photo
credit: Daniel Kronauer).
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phenotypes appears to be a common feature to clades of social insect symbionts (
Moore and Rob-
ertson, 2014
;
Parker and Grimaldi, 2014
), and presumably results from intense selection pressures
inside colonies (
Kistner, 1979
;
Parker, 2016
).
Promyrmister
adds further support to the view that
the earliest-known ants were socially complex (
Barden and Grimaldi, 2016
). Evidently, their colonies
were also resource rich enough for exploitation by impostor myrmecophiles, which we conclude
have been an unremitting part of ant biology. Despite their phenotypic intricacy and obligate depen-
dency on other species, complex behavioral relationships between animals can be extraordinarily
ancient, and persist over deep evolutionary time.
Materials and methods
Material and photography
This study is based on a single specimen of Burmese amber (CNU-008021) collected from Noije
Bum, Tanaing, Kachin, Myanmar. The specimen is housed at Key Laboratory of Insect Evolution and
Environmental Changes, Capital Normal University, Beijing. The holotype of the new genus and spe-
cies is embedded in a cuboid amber piece. The holotype was examined under a Leica M205C dis-
secting microscope and photographed using a Visionary Digital BK Lab Plus system (Austin, Texas).
The source images were aligned and stacked in Helicon Focus (Ukraine). Fluorescence images of the
fossil were made on a Zeiss LSM 880 (with Airyscan) confocal microscope (Germany) with a 488 nm
laser. Scanning electron microscopic images of
Haeterius
were obtained using a Tabletop Hitachi
Microscope TM3030Plus (Japan). Morphological terminology follows
S
́
lipin
́
ski and Mazur (1999)
,
Zhou et al. (2018)
, and
Caterino and Tishechkin (2015)
.
Taxon sampling, morphological characters and phylogenetic analysis
We scored
Promyrmister
for 259 external morphological characters used by
Caterino and Tishech-
kin (2015)
in a study investigating relationships among the tribe Exosternini, which is closely related
to Haeteriinae. From the original matrix, we selected all taxa from the nearest sister clades of Hae-
teriinae, including 35 taxa belonging to Exosternini, including all species of
Yarmister
(apparently the
closest genus to Haeteriinae;
Caterino and Tishechkin, 2015
). We also included representatives of
four other tribes: Omalodini, Histerini, Hololeptini and Platysomatini, and assigned
Hister unicolor
as
the primary outgroup, following
Caterino and Tishechkin (2015)
. The final taxon list is presented in
Supplementary file 2A
.
We also enlarged our data matrix by adding one more taxon (
Haeterius ferrugineus
) two more
characters (260 and 261), and one more state for Character 14:
260: Epistoma: (1) without depressions receiving scapes in repose, occasionally with small depres-
sions but without sharp arched-inwards epistomal striae; (2) with large depressions receiving scapes
in repose, often defined by sharp arched-inwards epistomal striae.
261: Arched-inwards epistomal striae: (1) convergent, but separated from each other in the mid-
dle; (2) convergent, and meeting each other in the middle; (3) inapplicable.
14: Epistoma, surface: 6) deeply depressed, with lateral ridges (=raised epistomal striae) aligned
with frontal stria.
The complete matrix of 46 taxa, 261 characters was constructed in Mesquite v. 3.20
(
Maddison and Maddison, 2016
); the matrix is provided in the nexus file (
Supplementary file 1
).
Bayesian analysis was carried out using MrBayes 3.2.6 (
Ronquist et al., 2012
) accessed via the
CIPRES Science Gateway Version 3 (
Miller et al., 2010
) (phylo.org). The Mkv model of character
evolution was used with a gamma distribution, and two MCMC were executed with four chains for
100 million generations. Convergence was judged to have occurred when the standard deviation of
split frequencies dropped below 0.005, and by ESS values higher than 200 in Tracer v1.7.0
(
Rambaut et al., 2018
), indicating adequate estimation of the posterior. The first 25% of trees were
discarded as burn-in. We used Treeannotator (
Bouckaert et al., 2014
) to obtain the maximum clade
credibility tree from post burn-in trees (ESS > 200) (
Figure 2A
), and added the estimated nodal
Bayesian posterior probability (BPP) in FigTree v1.4.3 (
https://github.com/rambaut/figtree/
). Parsi-
mony analysis was conducted in TNT Version 1.5 (
Goloboff and Catalano, 2016
) using Traditional
Search without, and with implied weighting setting (function K = 13 in
Figure 2—figure supple-
ments 2
and
3
). A consensus tree (
Figure 2B
; L = 1604, CI = 25, RI = 42) was obtained from four
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shortest-length trees (L = 1483, CI = 28, RI = 48) and the branch support was also calculated using
10,000 bootstrap replicates. Mapping character state changes onto the tree was performed in Win-
Clada (
Nixon, 2002
).
Host ant ages
A list of haeteriine host ant genera was obtained from the literature (
Helava et al., 1985
;
Ye
́
la-
mos, 1997
;
Tishechkin, 2007
;
Lapeva-Gjonova, 2013
;
Mazur, 1981
). To estimate ages of stem-
group and Recent host ant taxa in
Figure 3a
, data for earliest-known fossils were obtained from
Bar-
den (2016)
(
Barden, 2016
;
Barden, 2018
), and molecular age estimates of crown-groups were
taken from recent taxon-specific phylogenetic studies (
Borowiec et al., 2017a
;
Borowiec et al.,
2017b
;
Blaimer et al., 2015
;
Ward et al., 2015
;
Ferguson-Gow et al., 2014
;
Ward et al., 2010
;
Schmidt, 2013
). Data are presented in
Supplementary file 2B
.
Nomenclatural acts
This published work and the nomenclatural acts it contains have been registered in ZooBank, the
online registration system for the International Code of Zoological Nomenclature. The ZooBank
LSIDs (Life Science Identifiers) can be resolved and the associated information viewed through any
standard web browser by appending the LSID to the prefix ‘http://zoobank.org/’. The LSIDs for this
publication are to be found at:
urn:lsid:zoobank.org:pub:4AE2E535-B2B7-4A9A-829F-FA17CB98AD9C.
The specific LSIDs for new nomenclatural acts:
Genus: urn:lsid:zoobank.org:act:8125C3AB-A6C3-41AF-A9D7-0B67BBA2ACAD
Species: urn:lsid:zoobank.org:act:56DE873C-0163–4 F94-8D09-196F20B84C57
Data availability
All data generated or analyzed during this study are included in this published article (and its Sup-
plementary Information files). The holotype specimen of
Promyrmister kistneri
is housed at Key Lab-
oratory of Insect Evolution and Environmental Changes, Capital Normal University, Beijing (accession
number CNU-008021).
Acknowledgements
We are grateful to Alexey K Tishechkin (USDA), Michael S Caterino (Clemson University) and Alfred
Newton (Field Museum) for their helpful advice on the placement of the fossil and to Margaret K
Thayer (Field Museum) for a very thorough review of the paper. Phil Barden (New Jersey Insitute of
Technology) provided invaluable insight into the ant fossil record and possible hosts of
Promyrmis-
ter
. This research was supported by a Shurl and Kay Curci Foundation Research Grant, a Rita Allen
Scholars Award and a Klingenstein-Simons Fellowship Award in the Neurosciences to JP, and the
National Natural Science Foundation of China Grant no. 31402008 and International Postdoctoral
Exchange Fellowship no. 20150064 to YLZ. Rolf Oberprieler (ANIC) and Hong Pang (Sun Yat-Sen
University) helped with the fossil preparation, Lauren Ashman (ANIC) provided advice on improving
the manuscript and Cate Lemann (CSIRO) provided technical assistance.
Additional information
Funding
Funder
Grant reference number Author
National Natural Science
Foundation of China
31402008
Yu-Lingzi Zhou
International Postdoctoral Ex-
change Fellowship
20150064
Yu-Lingzi Zhou
Rita Allen Foundation
Joseph Parker
Zhou
et al
. eLife 2019;8:e44985.
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Evolutionary Biology
Esther A. and Joseph Klingen-
stein Fund
Joseph Parker
Shurl & Kay Curci Foundation
Joseph Parker
Simons Foundation
Joseph Parker
The funders had no role in study design, data collection and interpretation, or the
decision to submit the work for publication.
Author contributions
Yu-Lingzi Zhou, Conceptualization, Data curation, Formal analysis, Investigation, Visualization, Meth-
odology, Writing—original draft, Writing—review and editing; Adam S
́
lipin ́ski, Conceptualization,
Resources, Data curation, Formal analysis, Funding acquisition, Investigation, Visualization, Method-
ology, Writing—original draft, Project administration, Writing—review and editing; Dong Ren,
Resources, Funding acquisition, Project administration; Joseph Parker, Conceptualization, Resources,
Data curation, Formal analysis, Validation, Investigation, Visualization, Methodology, Writing—origi-
nal draft, Project administration, Writing—review and editing
Author ORCIDs
Joseph Parker
http://orcid.org/0000-0001-9598-2454
Decision letter and Author response
Decision letter
https://doi.org/10.7554/eLife.44985.016
Author response
https://doi.org/10.7554/eLife.44985.017
Additional files
Supplementary files
.
Supplementary file 1. Complete matrix of 46 taxa, 261 characters constructed in Mesquite v. 3.20.
DOI: https://doi.org/10.7554/eLife.44985.012
.
Supplementary file 2. Histerid taxa sampled for phylogenetic analysis, and ages of haeteriine host
ant genera inferred from fossil and molecular data.
DOI: https://doi.org/10.7554/eLife.44985.013
.
Transparent reporting form
DOI: https://doi.org/10.7554/eLife.44985.014
Data availability
All data generated or analyzed during this study are included in the manuscript and supporting files.
Source data for Figure 2, Figure 2 figure supplement 2 and Figure 2 figure supplement 3 are pro-
vided in Supplementary File 1.
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