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Quantifying the unquantifiable: Why Hymenoptera, not Coleoptera, is the most speciose animal order

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Abstract

Background: We challenge the oft-repeated claim that the beetles (Coleoptera) are the most species-rich order of animals. Instead, we assert that another order of insects, the Hymenoptera, is more speciose, due in large part to the massively diverse but relatively poorly known parasitoid wasps. The idea that the beetles have more species than other orders is primarily based on their respective collection histories and the relative availability of taxonomic resources, which both disfavor parasitoid wasps. Though it is unreasonable to directly compare numbers of described species in each order, the ecology of parasitic wasps-specifically, their intimate interactions with their hosts-allows for estimation of relative richness. Results: We present a simple logical model that shows how the specialization of many parasitic wasps on their hosts suggests few scenarios in which there would be more beetle species than parasitic wasp species. We couple this model with an accounting of what we call the "genus-specific parasitoid-host ratio" from four well-studied genera of insect hosts, a metric by which to generate extremely conservative estimates of the average number of parasitic wasp species attacking a given beetle or other insect host species. Conclusions: Synthesis of our model with data from real host systems suggests that the Hymenoptera may have 2.5-3.2× more species than the Coleoptera. While there are more described species of beetles than all other animals, the Hymenoptera are almost certainly the larger order.
Forbesetal. BMC Ecol (2018) 18:21
https://doi.org/10.1186/s12898-018-0176-x
CORRESPONDENCE
Quantifying theunquantiable: why
Hymenoptera, notColeoptera, isthemost
speciose animal order
Andrew A. Forbes*, Robin K. Bagley, Marc A. Beer, Alaine C. Hippee and Heather A. Widmayer
Abstract
Background: We challenge the oft-repeated claim that the beetles (Coleoptera) are the most species-rich order
of animals. Instead, we assert that another order of insects, the Hymenoptera, is more speciose, due in large part
to the massively diverse but relatively poorly known parasitoid wasps. The idea that the beetles have more species
than other orders is primarily based on their respective collection histories and the relative availability of taxonomic
resources, which both disfavor parasitoid wasps. Though it is unreasonable to directly compare numbers of described
species in each order, the ecology of parasitic wasps—specifically, their intimate interactions with their hosts—allows
for estimation of relative richness.
Results: We present a simple logical model that shows how the specialization of many parasitic wasps on their hosts
suggests few scenarios in which there would be more beetle species than parasitic wasp species. We couple this
model with an accounting of what we call the “genus-specific parasitoid–host ratio from four well-studied genera of
insect hosts, a metric by which to generate extremely conservative estimates of the average number of parasitic wasp
species attacking a given beetle or other insect host species.
Conclusions: Synthesis of our model with data from real host systems suggests that the Hymenoptera may have
2.5–3.2× more species than the Coleoptera. While there are more described species of beetles than all other animals,
the Hymenoptera are almost certainly the larger order.
Keywords: Beetles, Inordinate fondness, Animal diversity, Parasitic wasps, Parasitoids, Species richness
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…if the micro-hymenopterists would get off their lazy
asses and start describing species, there would be more
micro-Hymenoptera than there are Coleoptera.
Terry Erwin (in [1])
Background
e beetles (order Coleoptera), have historically [2,
3] and more recently [47] been described as the most
speciose order of animals on Earth. e great diversity
of beetles was sufficiently established by the middle of
last century such that Haldane (possibly apocryphally)1
quipped that an intelligent creator of life must have had
…an inordinate fondness for beetles” [8]. However, what
evidence underlies the claim that the Coleoptera are
more species-rich than the other insect orders? Certainly,
more species of beetles (> 350,000) have been described
than any other order of animal, insect or otherwise [11,
12], but does this reflect their actual diversity relative to
other insects? ough this may seem purely an academic
question, its resolution informs our understanding of
Open Access
BMC Ecology
*Correspondence: andrew-forbes@uiowa.edu
Department of Biology, University of Iowa, 434 Biology Building, Iowa
City, IA 52242, USA
1 Whether or not Haldane ever actually said it exactly in this way is unre-
solved [8, 9]. is phrase does not occur in any of Haldane’s writing, but he
does write that “e Creator would appear as endowed with a passion for
stars, on the one hand, and for beetles on the other” [10].
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Forbesetal. BMC Ecol (2018) 18:21
patterns and mechanisms of insect evolution (e.g., [13
15]) and, to the extent that species richness is a proxy
for ecological import [16, 17], how conservation efforts
might best be directed.
Why are beetles thought to be so diverse in the first
place? In part, historical biases in beetle collecting and an
associated accumulation of taxonomic resources for the
Coleoptera may have had an outsized influence on our
perception of diversity. In the mid-to-late 1800s, beetles
were prized among insects for their collectability. Many
gentlemen of leisure—including, notably, Charles Dar-
win—collected beetles for sport and would make a great
show of comparing the sizes of their respective collec-
tions [18, 19]. is preconception was then reinforced by
studies that extrapolated from specific, targeted collec-
tions of insect diversity that focused on beetles. Of these,
perhaps the highest in profile was a study conducted by
Terry Erwin. Erwin [20] used an insecticide to fog the
canopies of 19 individual Luehea seemannii trees in a
Panamanian rainforest and then collected and identified
the insect species that fell out of those trees. After hav-
ing identified the proportion of the beetle species that
were apparently host-specific to L. seemannii (163 of
955), he estimated that there might be as many as 12.2
million beetle species in the tropics. Similar studies seek-
ing to estimate global insect diversity have also tended to
emphasize beetles (e.g., [21, 22]).
Nevertheless, some previous work has challenged the
canon, with various authors suggesting—though never
quite insisting—that the Hymenoptera may be more spe-
ciose than the Coleoptera [2326]. e premise behind
this suggestion is that most of the larvae of the Parasit-
ica (one of the two infraorders of apocritan Hymenop-
tera; the other is the Aculeata, which includes ants, bees,
and stingingwasps), are obligate parasites of insect and
other arthropod hosts that feed on the host’s tissue until
the host dies ( “parasitoids”). Why is this parasitic life
history relevant to the Hymenoptera’s proportional con-
tribution to insect diversity? Simply put, species of par-
asitoid Hymenoptera (including the Parasitica, as well
as some other groups such as the Orussidae and some
Chrysidoidea) attack all orders of insects as well as some
non-insect arthropods [2729], and, reciprocally, most
holometabolous insect species are attacked by at least
one—and often many more than one—species of hyme-
nopteran parasitoid [30, 31]. For instance, Hawkins and
Lawton [32] examined parasitoid communities associ-
ated with 158 genera of British insects across five dif-
ferent orders, and found that parasitoid species richness
ranged from 2.64 to 9.40 per host species across different
host insect orders.
If parasitoid wasps are ubiquitous and most hosts are
attacked by many different species, why is there any
debate at all about the Hymenoptera being more diverse
than other orders? One reason may be that estimates of
the regional and global species-richness of parasitoid
wasps remain elusive. eir small size and a relative
paucity of taxonomic resources have left the parasitoid
Hymenoptera relatively under-described compared to
other insect orders [25, 33]. As a consequence, when col-
lection-based estimates of regional insect diversity have
been attempted, they have often excluded all but the larg-
est and easiest-to identify families of parasitic Hymenop-
tera (e.g., [3436]; though see [37, 38]).
A second reason for uncertainty regarding the spe-
cies richness of the parasitoid Hymenoptera is that their
host ranges are often unknown. While it may be true that
most insects harbor many parasitoid species, the ques-
tion remains whether these parasitoid communities are
exclusively composed of oligophagous or polyphagous
wasps that attack many hosts, or if instead the aver-
age insect host tends to have some number of specialist
Fig. 1 An illustration of how uncertainty about specialist vs. generalist behaviours might lead to misleading conclusions about parasitoid species
richness. In a, each host species (differently colored beetles) is attacked by two parasitoids. However, because all parasitoids attack all four beetles
the overall species richness of hosts exceeds that of the parasitoids (i.e., P:H < 1). In b, while some hosts have only one parasitoid, overall parasitoid
richness exceeds host richness (P:H > 1) because some parasitoids are more specialized
Page 3 of 11
Forbesetal. BMC Ecol (2018) 18:21
wasps among its many predators (Fig.1). Only in the lat-
ter case would one be able to confidently assert that the
Hymenoptera is the largest of the insect orders.
How then to approach this question without asking the
micro-hymenopterists (and the coleopterists, dipterists,
lepidopterists, etc.) to hurry up and describe all of the
world’s insect species? We suggest two complementary
approaches: (1) mathematically describing the values of
parasitoid-to-host (“P:H”) ratios that would support—or
contradict—the notion that the Hymenoptera is the most
speciose insect order and (2) tabulating—wherever pos-
sible—actual P:H ratios for various genera of host insects.
What parasitoid‑to‑host ratios would suggest
thattheHymenoptera are more species‑rich
thanother insect orders?
For the Hymenoptera to be the largest order of insects,
the global ratio of wasp parasitoids to hosts (P:H) need
not—in fact—equal or exceed 1.0. Indeed, a global P:H
of 1.0 (i.e., an average of one unique hymenopteran para-
sitoid species for each other insect species) would mean
that parasitoids account for a full half of all insects.
Instead, P:H ratios need only reach values such that the
Hymenoptera are more species-rich than the next largest
order (which, for the sake of argument, we will assume is
the Coleoptera). Here, we work towards finding param-
eters that describe that space. First, it will be true that:
where P is the proportion of all insect species that are
parasitoid Hymenoptera, C is the proportion of insects
that are Coleoptera, and I is the remaining proportion
of insect species, including the non-parasitoid Hyme-
noptera (Fig.2a). Note that for the sake of simplicity we
entirely exclude the many Hymenoptera that are parasitic
on other parasitoids (“hyperparasitoids”).
Additionally, because of the intimate relationship
between parasitoids and their hosts, we can describe the
(1)
I
=
1
(P
+
C)
Fig. 2 Representations of the space where the number of parasitoid wasp species would outnumber the Coleoptera, given different
parasitoid-to-host ratios for coleopteran hosts and for other insect hosts. a Pictorial representation of the model, wherein the total number of
parasitoid species (P) will be the sum of the number of species of Coleoptera (C) and of other insects (I), each first multiplied by their respective
overall parasitoid-to-host ratio (
pC
or
pI
); b black lines show results of the model for four different values of
pI
and with
pC
held at zero (i.e., when the
average coleopteran has no specialist parasitoids). Where black lines overlap with gray shaded areas represents space where P > C; c results of four
different scenarios in which
pC
and
pI
are equal; d some additional combinations of
pC
and
pI
. Though both axes could continue to 1.0, some high
values of P and C are not mathematically possible or biologically likely, and at P or C values above 0.5 the question about relative species-richness
becomes moot
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Forbesetal. BMC Ecol (2018) 18:21
proportion of species that are parasitoid Hymenoptera
using the following expression:
where
pC
and
represent the mean P:H ratios for all
coleopterans and all non-coleopterans, respectively. e
true values of
pC
and
pI
are unknowable, but can be esti-
mated (see next section), and their use in this way allows
for exploration of the ranges of P:H ratios that would
result in different relative numbers of Hymenoptera and
Coleoptera. Equation2 again excludes hyperparasitoids,
as well as parasitoids of non-insect arthropods, which
makes P a conservative estimate of the proportion of
insect species that are parasitoids.
Given these two relationships, we can substitute Eq.1
into Eq.2:
Equation3 allows us to find the values of
pC
and
pI
that result in a P > C or vice versa. As shown in Fig.2, the
space where P > C includes a substantial area where
pC
or
pI
(or both) can be < 1. For instance, if the Coleoptera
make up 25% of all insects, as suggested by many con-
temporary authors [22, 39], a
pC
of only 0.25 (or one spe-
cies-specialist parasitoid for every four beetle species),
coupled with a
pI
of 0.50, results in P = C (and the many
tens of thousands of non-parasitoid Hymenoptera will
then tip the scale in their favor). Even if the Coleoptera
amount to 40% of the insects, which reflects the percent-
age of currently-described insect species that are beetles,
there will be more parasitoid Hymenoptera than beetles
if
pC
and
pI
are equal to or in excess of 0.67 (two special-
ist parasitoid species for every three host species).
Another way to explore the values of
pC
and
pI
at
which P will be greater than C is to find the circum-
stances when the two will be equal. If we substitute C for
P into Eq.3, we get:
We can then plot
pC
vs
for values of C between 0
and 0.5 (Fig.3). Here, each line represents circumstances
when P = C, such that the area above and to the right of
each line represents values of
pC
and
that result in a
P > C. Here again,
pC
and
need not be particularly
large for the parasitoid Hymenoptera to exceed the spe-
cies richness of the Coleoptera. For instance, if one quar-
ter of all insects are beetles,
pC
and
pI
need only exceed
0.4 (the equivalent of two parasitoid species for every five
host species).
(2)
P
=
C(pC)
+
I(pI),
(3)
P
=
C(pC)
+
pI
pI(P
+
C).
(4)
pC=1+2pI
pI
C
What doactual P:H ratios look likeinnature?
e next question becomes: can we estimate parasi-
toid: host ratios (e.g.,
pC,pI
) for different host insects?
Quantifying global P:H ratios for entire insect orders
is as unapproachable as the task of counting all of the
living insect species: not only are most Hymenop-
tera undescribed, host records for described species
are often incomplete, such that multiplying each host
species by its supposed number of specialist parasi-
toids may often inadvertently include parasitoids that
share hosts (Fig.4). While this is problematic, recog-
nition of the problem helps present paths forward.
For indeed, some host–parasitoid systems are exceed-
ingly well studied and well-understood, such that we
can be reasonably confident about the completeness
of the host records of at least some parasitoids. With
this information, we can calculate a metric that we call
the genus-specialist parasitoid:host ratio. is metric
interrogates all members of a host insect genus in the
same geographic region and identifies all of the para-
sitoids known to attack only members of that genus
(the “genus-specialist” parasitoids). Because this P:H
ratio ignores all parasitoids known to attack any extra-
generic host—as well as those whose host range is
Fig. 3 Plot based on Eq. 4, with five representations of circumstances
when C and P are equal proportions (solid black lines).
pI
= overall
P:H ratio for non-coleopteran insect hosts;
pC
= overall P:H ratio for
the Coleoptera. Space above and to the right of each line represents
values of
pC
and
pI
where P > C, while space below and to the left of
each line represents values where C > P
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Forbesetal. BMC Ecol (2018) 18:21
unknown or has been incompletely studied—it is there-
fore an extremely conservative estimate of the overall
P:H ratio for an insect genus.
Below, we present four case studies, representing host–
parasitoid systems with records sufficiently complete to
allow for calculation of genus-specialist parasitoid:host
ratios. For each system, we focus on a single host genus
in North America. We restricted geography so that
parasitoid numbers would not be inflated by large bio-
geographic differences between hosts in their parasitoid
assemblages. North America was chosen because sam-
pling is relatively strong, and several robust resources
exist for Nearctic parasitoids (e.g., [29, 40, 41]).
For each system, we searched for all literature that men-
tioned the name of the host genus (or historical synonyms)
and either “parasite” or “parasitoid” and compiled a data-
base of records, performing reticulated searches on each
parasitoid species name as it was added to the database in
order to determine known parasitoids host ranges. From
among all parasitoid records, we classified parasitoids as
“genus-specialists” if they had only ever been reared from
hosts in this same genus. We then split these “genus-spe-
cialists” into two groups: those for which an argument can
be made that they do not have unknown extra-generic
hosts, and those that were “possible genus-specialists” but
for which records were less complete. Non-hymenopteran
parasitoids (e.g., Tachinidae) were excluded, but in any
case were only present for two of the four hosts we exam-
ined (Malacosoma and Neodiprion), and generally do not
have the taxonomically cosmopolitan host ranges of the
hymenopteran parasitoids. For cases where host genera
were found on multiple continents, only host species in
North America were included in the study, and to be con-
servative, a parasitoid was still considered “generalist” if it
occurred on an extra-generic host species outside of North
America. Introduced host species were noted but not
counted in host lists, as they do not represent long-term
host–parasite relationships. Introduced parasitoid spe-
cies were included in generalist lists, regardless of whether
they were specialists on that genus in North America or
elsewhere. We describe each system below and refer the
reader to additional materials for species lists, specialist/
generalist classifications, and citations. A summary of data
across the four genera and references for these datacan be
found in Additional files 1and 2.
System 1: Rhagoletis (Diptera: Tephritidae)
Many North American Rhagoletis flies are pests of agri-
culturally-important fruits. Eggs are deposited in ripen-
ing fruits by the female fly, and larvae develop through
several instars while feeding on fruit pulp [42]. For most
species, larvae then exit the fruit and pupate in the soil.
Parasitoids are known from egg, larval and pupal stages of
many Rhagoletis species. Several studies have described
the parasitoid communities associated with Rhagoletis
agricultural pest species (e.g., [4246]), though records of
parasitoids of non-pest species also exist (e.g., [4749]).
Moreover, many of the associated parasitoid species are
well-studied in their own right, with robust records of
their biology, ecology, and host-ranges [45, 5052].
Of the 24 species of North American Rhagoletis flies,
16 have a published record of parasitoid associations.
Fig. 4 Known genus-specialist parasitoids can be used to calculate a minimum P:H ratio for an insect host genus. The focal beetle genus H (three
species) has four known parasitoids, P1–P4. P1 and P4 are relatively well-studied, and known to be genus-specialists, attacking only hosts in this
beetle genus. P3 has some known extra-generic hosts, while the host range of P2 is poorly studied and unknown extra-generic hosts may exist. For
the purposes of estimating a genus-specialist P:H, one would therefore use only P1 and P4, such that a minimum P:H for this beetle genus would
be 2/3, or 0.67. Note that if the total number and identities of extra-generic hosts were known for P2 and P3, a “true” P:H for the genus could be
calculated (see “Synthesis”)
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Forbesetal. BMC Ecol (2018) 18:21
Across these 16 flies, we found records of 39 parasitoid
species, among which 24 “genus-specialists” have been
described only from North American Rhagoletis and no
other insect host (Additional file1: TableS1). Of these,
we set aside three “possible” genus-specialist species that
did not have a strong collection record and for which
host records may possibly be incomplete. e remain-
ing set of genus-specialists included 14 braconids (genera
Diachasma, Diachasmimorpha, Utetes, and Opius), six
diapriids (genus Coptera), and a pteromalid (genus Hal-
ticoptera). e genus-specialist P:H ratio for Rhagoletis
is therefore either 1.31 (21/16), or 1.50 (24/16), depend-
ing on whether “possible genus-specialists” are included.
An extra-conservative P:H ratio might also include the
eight Rhagoletis hosts that have no record of parasitoids
(P:H = 21/24 = 0.88), though this almost certainly ignores
some number of unknown genus-specialist parasitoids.
Some of the 15 “generalist” parasitoids of Rhagole-
tis have been reared from a diverse set of extra-generic
hosts, but in some cases only from one other fruit-infest-
ing tephritid (e.g., Phygadeuon epochrae and Coptera
evansi, both of which have only been reared from Rhago-
letis and from Epochra canadensis [Diptera: Tephriti-
dae]). ese 15 “generalists” are listed in Additional file1:
TableS1.
System 2: Malacosoma (Lepidoptera: Lasiocampidae)
e tent caterpillars (genus Malacosoma) are shelter
building, cooperatively-foraging moths that damage both
coniferous and deciduous trees across at least 10 families.
Most species use > 1 host tree genus, though some (e.g.,
Malacosoma constrictum; Malacosoma tigris) are more
specialized [53]. ere are six North American species of
Malacosoma, some with overlapping geographic distri-
butions [53]. Female moths lay eggs in a mass wrapped
around a branch of the host tree. Larvae of most species
(M. disstria is an exception) live colonially inside “tents”
made of spun silk and make regular excursions to feed on
host leaves. e caterpillar stage is eaten by birds, mam-
mals and several insect predators, but the most taxonom-
ically diverse natural enemies are the parasitoids [53].
Of these, approximately one-third are Dipteran (family
Tachinidae), while the remaining two-thirds are Hyme-
nopteran parasitoids. Parasitoids attack all immature life
stages, but most appear to emerge during the pre-pupal
or pupal stage. Parasitoids of the North American tent
caterpillars have been well documented, and often in the
context of other available forest caterpillar hosts, such
that it is reasonable to assert that some parasitoid species
are Malacosoma-specific (e.g., [5456]).
All six of the North American Malacosoma species
have at least one known parasitoid association, and we
compiled a total of 78 different parasitoid species across
all hosts (Additional file1: TableS2). Of these, eleven had
only been reared from Malacosoma. Five of these eleven
species we assigned to the “possible genus-specialists”
category, as they had not been assigned a specific name
(which makes it hard to determine whether other hosts
exist), or because they had only been reared a single time
from the host. e remaining six “genus-specialists,” were
from four different hymenopteran families. e genus-
specialist P:H ratio for Malacosoma is therefore between
1.00 and 1.83.
Malacosoma have many more “generalists” than Rhago-
letis: 68 species have been reared from both Malacosoma
and at least one other extra-genetic host (Additional
file1: TableS2). Many of these appear to be specific to
Lepidopteran hosts.
System 3: Dendroctonus (Coleoptera: Curculionidae)
Approximately 14 species of Dendroctonus bark bee-
tles are found in North America [57]. Dendroctonus are
specific to conifers in family Pinaceae, and can be highly
destructive to their host trees. Female beetles construct
nuptial chambers in trees where they mate with males
and then deposit eggs in tunnels in the phloem. Larvae
feed on phloem and outer bark and leave the tree only
after pupation and adult emergence [57]. Most species
are tree genus- or species-specific.
Parasitoids have been described for eight of the 14
North American Dendroctonus species, though for two of
these (D. adjunctus and D. murryanae) only one or two
parasitoid species are known. e total list of Dendroc-
tonus-associated parasitoids is long, but the records are
also often problematic, as Dendroctonus share their habi-
tat with several other genera of bark beetles, which may
or may not be attacked by the same parasitoids. In many
studies, parasitoids are listed as “associates” of either
Dendroctonus, or of one of the other species, or of both,
but this does not always necessarily mean that a para-
sitoid attacks that beetle [5860]. We have here again
tried to be conservative, though in one case (Meterorus
hypophloei) we have ignored a claim of “association” with
Ips beetles [61] as it did not seem to be well justified and
other authors describe M. hypophloei as a Dendroctonus
frontalis specialist [60, 62]. In total, we found nine Den-
droctonus genus-specialists, two possible genus-special-
ists, and 48 “generalists” (Additional file1: TableS3). e
genus-specific P:H ratio for Dendroctonus is therefore
between 1.13 and 1.38.
System 4: Neodiprion (Hyemenoptera: Diprionidae)
Neodiprion is a Holarctic genus of pine-feeding sawflies
specializing on conifers in the family Pinaceae [63]. ese
sawflies have close, life-long associations with their tree
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Forbesetal. BMC Ecol (2018) 18:21
hosts. e short-lived, non-feeding adults mate on the
host plant shortly after eclosion, after which the females
deposit their eggs into pockets cut within the host nee-
dles. e larvae hatch and feed externally on the host
needles throughout development, and then spin cocoons
on or directly beneath the host [6466]. Many species
also have highly specialized feeding habits, and feed on a
single or small handful of host-plant species in the genus
Pinus. Since many of the ~ 33 Neodiprion species native
to North America are considered economic pests [67],
considerable effort has gone into describing their natu-
ral history and exploring potential methods to control
Neodiprion outbreaks.
Despite the wealth of natural history information,
compiling a list of parasitoids attacking Neodiprion is
complicated by a history of accidental and intentional
introductions. In addition to the native species, the Euro-
pean pine sawfly, Neodiprion sertifer, and three species
from the closely related genera Diprion and Gilpinia were
introduced in the past ~ 150years and have spread across
the United States and Canada [6871]. In an attempt to
control these invasive pests, several parasitoids have been
introduced, and now attack both native and invasive dip-
rionids [7274].
We found 20 genus-specialist parasitoid species associ-
ated with the 21 species of North American Neodiprion
for which parasitoid records exist. An additional seven
parasitoids were classified as “possible” genus-specialists.
e genus-specific P:H ratio for Neodiprion is therefore
between 0.95 and 1.29. An additional 51 species had been
reared from both Neodiprion and an extra-generic host,
with nine introduced parasitoids. We also compiled a
list of 14 introduced parasitoids, nine hyperparasitoids,
and 28 tachinid (Diptera) parasitoids of Neodiprion
(Additional file1: TableS4), but these were not included
in any analyses.
Synthesis
Upon considering our model together with actual esti-
mates of P:H ratios from natural host systems (Table1),
there appear to be few conditions under which the
Hymenoptera would not be the largest order of insects.
If, for instance, the P:H ratios for Rhagoletis, Malaco-
soma, Dendroctonus, and Neodiprion are at all repre-
sentative of other hosts in those respective orders, and
we use them to calculate relative species richness based
on recent counts of only the described species in each
order [75], the Hymenoptera exceed the Coleoptera by
2.5–3.2 times (Table 2). Recall that these calculations
ignore all hyperparasitoids, and also omit parasitoids of
other insect orders (e.g., Hemiptera, Orthoptera) and of
non-insect arthropods. Even if we use half of the lowest
P:H ratio estimate for each of the four largest orders, the
Hymenoptera would outnumber the Coleoptera by more
than 1.3 times.
Note that P:H ratios might be measured more accu-
rately and/or calculated in different ways, most of
which we would expect to increase the estimates of P:H
reported here. For instance, rather than ignoring all of
the so-called “generalist” parasitoids, one could identify
those for which host ranges are known (e.g., Fig.4), divide
each by the total number of host genera attacked, and
add that fraction to the numerator of the P:H ratio for the
focal host genus. As one example, the “generalist” para-
sitoids Phygadeuon epochrae and Coptera evansi both
attack only Rhagoletis flies and the currant fly Epochra
canadensis. ese would each add an additional 0.5 to
the other 24 “genus-specialist” parasitoids of Rhagoletis,
Table 1 Summary ofestimates ofparasitoid tohost (P:H) ratios forfour host insect genera
Shown for each host genus are: the total number of North American (NAm) species, as well as the number with parasitoid records; the overall P:H, which includes
generalist species; the genus-specialist P:H; and the genus-specialist P:H when “possible genus-specialists” were included. Parasitoid families that were among each
group of genus-specialists are also listed
Focal host genus # NAm species (#
withparasitoid
records)
P:H (overall) P:H (genus-
specialists
only)
P:H (specialist) [including
possible genus-
specialists]
Genus-specialist families
Rhagoletis (Diptera: Tephriti-
dae) 24 (16) 2.44 1.31 1.50 Braconidae; Diapriidae; Ptero-
malidae
Malacosoma (Lepidoptera:
Lasiocampidae) 6 (6) 13.00 1.00 1.83 Braconidae; Eulophidae; Ich-
neumonidae; Platygastridae
Dendroctonus (Coleoptera:
Curculionidae) 14 (8) 6.50 1.13 1.38 Braconidae; Ichneumonidae;
Gasteruptiidae; Proc-
totrupidae; Pteromalidae;
Platygastridae
Neodiprion (Hymenoptera:
Diprionidae) 33 (21) 3.48 0.95 1.29 Ichneumonidae; Chrysididae
Page 8 of 11
Forbesetal. BMC Ecol (2018) 18:21
giving a revised P:H of 1.56. For Malacosoma, Dendroc-
tonus, and Neodiprion, which all have many “generalist”
parasitoids with host ranges that include only a few other
extra-generic hosts in the same respective family, such
additions should increase P:H ratio estimates by a con-
siderable margin.
Another way to calculate P:H would be to focus not on
a host genus but on hosts sharing the same habitat. For
instance, Dendroctonus bark beetles share their habitat
niche with several other species of beetle, and many of
their parasitoids are “specialists” in the sense that they
attack more than one bark beetle, but all within the same
tree habitat [60]. One could, therefore, calculate a P:H
where H is the number of potential beetle host species
in the habitat, and P is the number of “habitat-specialist”
parasitoid species (those that attack one or more of the
hosts in that habitat and no other hosts in other habitats).
Our analyses largely ignore the increasingly common
finding that many apparently polyphagous insects—both
herbivores and parasitoids—show evidence of additional
host-associated genetic structure that might, if consid-
ered here as distinct lineages, change P:H ratios (e.g.,
[7681]). Indeed, all four of our focal host genera have
named subspecies or show evidence for host-associated,
reproductively-isolated lineages [57, 8284]. ough we
chose to “lump” subspecies and other reproductively iso-
lated lineages together for this analysis, it is interesting
to consider how a detailed study of genetic diversity and
reproductive isolation among a host genus and all of its
associated parasitoids might change P:H ratios. Studies of
the flies in the Rhagoletis pomonella species complex and
three of their associated parasitoids suggest that where
additional host-associated lineages are found in a phy-
tophagous insect, this cryptic diversity may be multiplied
many times over in its specialist parasitoid community
[51, 85]. If broadly true, this implies that genus-specific
P:H ratios may often be much higher than we report here.
One sensible criticism will surely be: to what extent are
the P:H ratios for these four genera reflective of global
P:H ratios for their respective orders (Coleoptera, Lepi-
doptera, Diptera, and the non-parasitoid Hymenoptera)?
Surely some insect genera escape parasitism, and per-
haps the examples chosen here simply have exceptionally
large, or unusually specialized, parasitoid communities.
As to the former, it may be that such escape artists exist,
but they also may be relatively rare. After all, there are
parasitoids that attack aquatic insects [86, 87], that para-
sitize insects in Arctic communities (e.g., [88]), and even
those that dig down into soils to unearth and oviposit
into pupae [50]. e list of potential hosts for parasitoids
also extends to many non-insect arthropods [89, 90]. As
to the four example genera being representative of overly
large parasitoid communities, all of their “overall” P:H
numbers (Table1) are actually below the means found for
their respective orders in an extensive study of parasitoid
communities in Britain [32], suggesting that these com-
munities are of average, or slightly below-average, size.
A second, equally sensible, criticism is that a sample
size of four offers only a limited glimpse of genus-spe-
cialist P:H ratios, and that the same data should be col-
lected from additional host insect genera. Having started
out with a list of nearly 50 potential host genera and find-
ing host–parasitoid records to be inadequate for all but
four, we wholeheartedly agree. ere is a great need to
Table 2 Calculations of hymenopteran species richness, given numbers of described insect species in other orders
andP:H ratios estimated inthis paper
Combining conservative P:H ratio estimates from four case studies with numbers of described species in the four largest insect orders [33, 75] oers an idea of how
species richness of the Hymenoptera may compare with that of other orders
a Parastioids attack hosts in all other insect orders, but these are omitted as we did not estimate P:H ratios for any hosts in these orders. Total numbers therefore
exclude large numbers of hymenopteran species
High P:H estimates fromcase
studies Low P:H estimates fromcase
studies Half oflowest
estimates fromcase
studies
Diptera (152,244) 228,366 199,440 99,720
Lepidoptera (156,793) 286,931 156,793 78,397
Coleoptera (359,891) 494,850 406,677 203,338
Non-parasitoid Hymenoptera (~ 62,000) 79,980 58,900 29,450
All other insect orders (335,970) 0a0a0a
Total parasitoid Hymenoptera 1,107,487 833,590 416,795
Non-parasitoid Hymenoptera (to add to calculated
parasitoid numbers) 62,000 62,000 62,000
Total Hymenoptera 1,152,127 883,810 472,905
Page 9 of 11
Forbesetal. BMC Ecol (2018) 18:21
assemble datasets of the type presented here for addi-
tional hosts, including from insects using other feeding
niches, from other insect orders, and from insects out-
side of North America, especially in tropical forests. In
the future, perhaps a more comprehensive analysis of P:H
ratios will be possible.
Concluding thoughts
While it may indeed be premature to claim that the
Hymenoptera is the largest order of insects based solely
on our data, many other studies offer support for the
same conclusion. In fact, the preponderance of evidence
suggests that the common wisdom about the Coleop-
tera being the most speciose is the more dubious claim.
Studies of insect diversity that reduce taxonomic biases
have found the Hymenoptera to be the most species-rich
in both temperate [37] and tropical [38] forests, as well
as in other habits (e.g., [91, 92]) and across the entirety
of the British Isles [17]. In addition, a mass-barcoding
study of Canadian insects found both Hymenoptera and
Diptera were more diverse than Coleoptera [93]. After
Hymenoptera, the Coleoptera may not even be the sec-
ond most-speciose order; several recent inventories of
species diversity suggest that the Diptera may hold that
title [17, 94, 95]. Moreover, other historically-accepted
ideas about diversity of parasitoid hymenopterans have
recently been questioned, including the apparent myth
that parasitoids are one of only a few groups whose diver-
sity decreases towards the tropics [9698]. In any case,
we hope this commentary results in a redoubled effort to
understand and describe the ecology and natural histo-
ries of parasitoid wasps, including host ranges and cryp-
tic host-associated diversity, such that estimates of P:H
can be made for additional host genera. We also hope to
see similar efforts in other animal groups that may har-
bor great diversity but for which far too little is known
about host ranges, such as in some particularly speciose
orders of mites and nematodes (e.g., [99, 100]. In other
words, and to again quote Erwin [20], we hope that “…
someone will challenge these figures with more data.
Authors’ contributions
AAF conceived of the study. All authors helped formulate a framework for
addressing the questions in the paper, developed the logical model, and col-
lected and analyzed data from the four host genera. AAF and RKB wrote the
manuscript. All authors read and approved the final manuscript.
Additional les
Additional le1: Tables S1–S4. Parasitoid lists used in genus-specialist
P:H ratio calculations.
Additional le2. References for parasitoid lists in Tables S1–S4.
Acknowledgements
We thank Isaac Winkler, Anna Ward, Eric Tvedte, Miles Zhang, Glen Hood, and
Matt Yoder for their thoughtful discussions and comments on this manuscript.
Peter Mayhew and two anonymous reviewers provided helpful suggestions
for improving the manuscript, particularly with regard to future directions.
Competing interests
The authors declare that they have no competing interests.
Availability of data and materials
The datasets supporting the conclusions of this article are included within the
article and its additional files.
Consent for publication
Not applicable.
Ethics approval and consent to participate
Not applicable.
Funding
Projects funded by the National Science Foundation to AAF (DEB 1145355 and
1542269) led directly to the discussions that motivated this study.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in pub-
lished maps and institutional affiliations.
Received: 24 March 2018 Accepted: 13 June 2018
References
1. Rice ME, Terry L. Erwin: she had a black eye and in her arm she held a
skunk. Zookeys. 2015;500:9–24.
2. Kirby W, Spence W. An introduction to entomology. London: Longman,
Hurt, Rees, Orme, and Brown; 1818.
3. Hutchinson GE. Homage to Santa Rosalia or why are there so many
kinds of animals? Am Nat. 1959;93:145–59.
4. Oberprieler RG, Marvaldi AE, Anderson RS. Weevils, weevils, weevils
everywhere. Zootaxa. 2007;1668:491–520.
5. McKenna D, Farrell BD. Beetles (Coleoptera). In: Hedges S, Kumar S,
editors. The timetree of life. Oxford: Oxford University Press; 2009. p.
278–89.
6. Zhang ZQ. Animal biodiversity: an introduction to higher-level clas-
sification and taxonomic richness. Zootaxa. 2011;12:7–12.
7. Zhang S-Q, Che L-H, Li Y, Liang Dan, Pang H, Ślipiński A, et al. Evolution-
ary history of Coleoptera revealed by extensive sampling of genes and
species. Nat Commun. 2018;9:205.
8. Gould S. A special fondness for beetles. Nat Hist. 1993;102:4–8.
9. Williamson M. Haldane’s special preference. Linn. 1992;8:12–5.
10. Haldane J. What is life? The Layman’s view of nature. London: Lindsay
Drummond; 1949.
11. Farrell BD. “Inordinate fondness” explained: why are there so many
beetles? Science. 1998;281:555–9.
12. Bouchard P, Grebennikov VV, Smith ABT, Douglas H. Biodiversity of
Coleoptera. In: Foottit RG, Adler PH, editors. Insect biodiversity: science
and society. Oxford: Wiley-Blackwell; 2009. p. 265–301.
13. Mayhew PJ. Shifts in hexapod diversification and what Haldane could
have said. Proc Biol Sci. 2002;269:969–74.
14. Wiens JJ, Lapoint RT, Whiteman NK. Herbivory increases diversification
across insect clades. Nat Commun. 2015;6:8370.
15. Ferns PN, Jervis MA. Ordinal species richness in insects-a preliminary
study of the influence of morphology, life history, and ecology. Entomol
Exp Appl. 2016;159:270–84.
16. May RM. How many species are there on Earth? Science.
1988;241:1441–9.
17. Shaw MR, Hochberg ME. The neglect of parasitic Hymenoptera in insect
conservation strategies: the British fauna as a prime example. J Insect
Conserv. 2001;5:253–63.
Page 10 of 11
Forbesetal. BMC Ecol (2018) 18:21
18. Browne J. Charles Darwin: voyaging. Princeton: Princeton University
Press; 1996.
19. Sheppard CA. Benjamin Dann Walsh: pioneer entomologist and propo-
nent of Darwinian theory. Annu Rev Entomol. 2004;49:1–25.
20. Erwin TL. Tropical forests: their richness in Coleoptera and other arthro-
pod species. Coleopt Bull. 1982;36:74–5.
21. Ødegaard F. How many species of arthropods? Erwin’s estimate revised.
Biol J Linn Soc. 2000;71:583–97.
22. Stork NE, McBroom J, Gely C, Hamilton AJ. New approaches narrow
global species estimates for beetles, insects, and terrestrial arthropods.
Proc Natl Acad Sci USA. 2015;112:7519–23.
23. LaSalle J. Parasitic Hymenoptera, biological control and biodiversity. In:
LaSalle J, Gauld ID, editors. Hymenoptera and biodiversity. Wallingford:
CAB International; 1993. p. 197–215.
24. LaSalle J, Gauld ID. Hymenoptera: their diversity, and their impact on
the diversity of other organisms. In: LaSalle J, Gauld ID, editors. Hyme-
noptera and biodiversity. Wallingford: CAB International; 1993. p. 1–26.
25. Gaston KJ. Spatial patterns in the description and richness of the Hyme-
noptera. In: LaSalle J, Gauld ID, editors. Hymenoptera and biodiversity.
Wallingford: CAB International; 1993. p. 277–93.
26. Austin AD, Dowton M. Hymenoptera: evolution, biodiversity, and
biological control. Clayton: CSIRO Publishing; 2000.
27. Gibson GAP, Huber JT, Woolley JB. Annotated Keys to the Genera of
Nearctic Chalcidoidea (Hymenoptera). Ottawa: NRC Research Press;
1997.
28. Wharton R, Marsh P, Sharkey M. Manual of the New World genera of the
family Braconidae (Hymenoptera). Spec Publ Int Soc Hymenopterists.
1997;1:1–439.
29. Noyes J. Universal Chalcidoidea Database. 2017. http://www.nhm.ac.uk/
chalc idoid s. Accessed 21 Mar 2018.
30. Schoenly K. The predators of insects. Ecol Entomol. 1990;15:333–45.
31. Memmott J, Godfray HCJ. Parasitoid webs. In: Lasalle J, Gauld ID, editors.
Hymenoptera and biodiversity. Wallingford: CAB International; 1993. p.
217–34.
32. Hawkins BA, Lawton JH. Species richness for parasitoids of British phy-
tophagous insects. Nature. 1987;326:788–90.
33. Huber JT. Biodiversity of Hymenoptera. In: Foottit RG, Adler PH, editors.
Insect biodiversity: science and society. Oxford: Wiley; 2009. p. 303–23.
34. Novotny V, Basset Y, Miller SE, Weiblen GD, Bremer B, Cizek L, et al.
Low host specificity of herbivorous insects in a tropical forest. Nature.
2002;416:841–4.
35. Pietsch TW, Bogatov VV, Amaoka K, Zhuravlev YN, Barkalov VY, Gage S,
et al. Biodiversity and biogeography of the islands of the Kuril Archi-
pelago. J Biogeogr. 2003;30:1297–310.
36. Basset Y, Cizek L, Cuénoud P, Didham RK, Guilhaumon F, Missa O, et al.
Arthropod diversity in a tropical forest. Science. 2012;338:1481–4.
37. Gaston KJ. The magnitude of global insect species richness. Conserv
Biol. 1991;5:283–96.
38. Stork NE. The composition of the arthropod fauna of Bornean lowland
rain forest trees. J Trop Ecol. 1991;7:161–80.
39. Hamilton AJ, Novotný V, Waters EK, Basset Y, Benke KK, Grimbacher
PS, et al. Estimating global arthropod species richness: refining
probabilistic models using probability bounds analysis. Oecologia.
2013;171:357–65.
40. Peck O. A catalogue of the Nearctic Chalcidoidea (Insecta: Hymenop-
tera). Mem Entomol Soc Canada. 1963;95:5–1092.
41. Krombein K, Hurd P, Smith D, Burks B. Catalog of Hymenoptera in
America North of Mexico. Washington, D.C.: Smithsonian Institution
Press; 1979.
42. Bush GL. The taxonomy, cytology, and evolution of the genus Rhago-
letis in North America (Diptera, Tephritidae). Bull Museum Comp Zool.
1966;134:431–562.
43. Lathrop F, Newton R. The biology of Opuis melleus Gahan, a parasite of
the blueberry maggot. J Agric Res. 1933;46:143–60.
44. Cameron P, Morrison F. Psilus sp. (Hymenoptera: Diapriidae), a parasite
of the pupal stage of the apple maggot, Rhagoletis pomonella (Diptera:
Tephritidae) in south-western Quebec. Phytoprotection. 1974;55:13–6.
45. Wharton RA, Marsh PM. New World Opiinae (Hymenoptera: Braconidae)
parasitic on Tephritidae (Diptera). J Washingt Acad Sci. 1978;68:147–67.
46. Feder JL. The effects of parasitoids on sympatric host races of Rhagoletis
pomonella (Diptera: Tephritidae). Ecology. 1995;76:801–13.
47. Rull J, Wharton R, Feder JL, Guillén L, Sivinski J, Forbes A, et al. Latitu-
dinal variation in parasitoid guild composition and parasitism rates
of North American hawthorn infesting Rhagoletis. Environ Entomol.
2009;38:588–99.
48. Forbes AA, Hood GR, Feder JL. Geographic and ecological overlap of
parasitoid wasps associated with the Rhagoletis pomonella (Diptera:
Tephritidae) species complex. Ann Entomol Soc Am. 2010;103:908–15.
49. Forbes AA, Satar S, Hamerlinck G, Nelson AE, Smith JJ. DNA barcodes
and targeted sampling methods identify a new species and cryptic pat-
terns of host specialization among North American Coptera (Hymenop-
tera: Diapriidae). Ann Entomol Soc Am. 2012;105:608–12.
50. Muesebeck C. The Nearctic parasitic wasps of the genera Psilus Panzer
and Coptera Say (Hymenoptera, Proctotrupoidea, Diapriidae). Technical
Bulletin 1617. Washington, D.C.: United States Department of Agriculture
Science and Education Administration; 1980.
51. Forbes AA, Powell THQ, Stelinski LL, Smith JJ, Feder JL. Sequential sym-
patric speciation across tropic levels. Science. 2009;323:776–9.
52. Wharton R, Yoder M. Parasitoids of fruit-infesting Tephritidae. 2017.
http://paroffi t.org. Accessed 20 Mar 2018.
53. Fitzgerald TD. The tent caterpillars. Ithaca: Cornell University Press; 1995.
54. Langston RL. A synopsis of hymenopterous parasites of Malacosoma in
California (Lepidoptera, Lasiocampidae). In: Lingsley E, Smith R, Stein-
haus E, Usinger R, editors. University of California publications entomol-
ogy, vol. 14. Berkeley: University of California Press; 1957. p. 1–50.
55. Stacey L, Roe R, Williams K. Mortality of eggs and pharate larvae of
the eastern tent caterpillar, Malacosoma americana (F.) (Lepidoptera:
Lasiocampidae). J Kansas Entomol Soc. 1975;48:521–3.
56. Shaw S. Aleiodes wasps of eastern forests: a guide to parasitoids and
associated mummified caterpillars. FHTET-2006-08. Washington, D.C.:
United States Department of Agriculture Forest Service, Forest Health
Technology Enterprise Team; 2006.
57. Six DL, Bracewell R. Dendroctonus. In: Vega FE, Hofstetter RW, editors.
Bark beetles: biology and ecology of native and invasive species.
Oxford: Academic Press; 2015. p. 305–50.
58. Overgaard N. Insects associated with southern pine beetle in Texas,
Louisiana, and Mississippi. J Econ Entomol. 1968;61:1197–201.
59. Langor DW. Arthropods and nematodes co-occurring with the eastern
larch beetle, Dendroctonus simplex [Col.: Scolytidae], in Newfoundland.
Entomophaga. 1991;36:303–13.
60. Berisford CW. Parasitoids of the southern pine beetle. In: Coulson R,
Klepzig K, editors. South Pine Beetle II General Tech Rep SRS-140. Ashe-
ville: United States Department of Agriculture Forest Service, Southern
Research Station; 2011. p. 129–39.
61. Kulhavy D, Goyer RA, Bing JW, Riley M. Ipps spp. natural enemy relation-
ships in the Gulf Coastal states. Stephen F Austin State Univ Fac Publ.
1989;300:157–67.
62. Stein CR, Coster JE. Distribution of some predators and parasites
of southern pine beetle in two species of pine. Environ Entomol.
1977;6:689–94.
63. Smith DR. Systematics, life history, and distribution of sawflies. Sawfly
life history adaptations to woody plants. San Diego: Academic Press;
1993. p. 3–32.
64. Coppel HC, Benjamin DM. Bionomics of the nearctic pine-feeding
Diprionids. Annu Rev Entomol. 1965;10:69–96.
65. Knerer G, Atwood CE. Diprionid sawflies: polymorphism and speciation.
Science. 1973;179:1090–9.
66. Knerer G. Life history diversity in sawflies. In: Wagner MR, Raffa KF,
editors. sawfly life history adaptations to woody plants. San Diego:
Academic Press; 1993. p. 33–60.
67. Arnett RH. American Insects: a handbook of the insects of America
North of Mexico. Gainesville: Sandhill Crane Press; 1993.
68. Britton W. A destructive pine sawfly introduced from Europe, Diprion
(Lophyrus) simile Hartig. J Econ Entomol. 1915;8:379–82.
69. Gray D. Notes on the occurrence of Diprion frutetorum Fabr. in southern
Ontario. Annu Rep Entomol Soc Ontario. 1938;68:50–1.
70. Balch R. The outbreak of the European spruce sawfly in Canada
and some important features of its bionomics. J Econ Entomol.
1939;32:412–8.
71. Schaffner JV Jr. Neodiprion sertifer (Geoff.), a pine sawfly acciden-
tally introduced into New Jersey from Europe. J Econ Entomol.
1939;32:887–8.
Page 11 of 11
Forbesetal. BMC Ecol (2018) 18:21
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72. Finlayson LR, Reeks WA. Notes on the introduction of Diprion parasites
to Canada. Can Entomol. 1936;68:160–6.
73. Finlayson T. Taxonomy of cocoons and puparia, and their contents, of
Canadian parasites of some native Diprionidae (Hymenoptera). Can
Entomol. 1963;95:475–507.
74. MacQuarrie CJK, Lyons DB, Lukas Seehausen M, Smith SM. A history
of biological control in Canadian forests, 1882–2014. Can Entomol.
2016;148:S239–69.
75. Adler PH, Foottit R. Introduction. In: Foottit R, Adler P, editors. Insect
biodiversity: science and society. Oxford: Wiley; 2009. p. 1–6.
76. Drès M, Mallet J. Host races in plant-feeding insects and their
importance in sympatric speciation. Philos Trans R Soc B Biol Sci.
2002;357:471–92.
77. Abrahamson WG, Blair CP, Eubanks MD, Morehead SA. Sequential radia-
tion of unrelated organisms: the gall fly Eurosta solidaginis and the tum-
bling flower beetle Mordellistena convicta. J Evol Biol. 2003;16:781–9.
78. Stireman JO, Nason JD, Heard SB, Seehawer JM. Cascading host-asso-
ciated genetic differentiation in parasitoids of phytophagous insects.
Proc R Soc B Biol Sci. 2006;273:523–30.
79. Smith MA, Rodriguez JJ, Whitfield JB, Deans AR, Janzen DH, Hallwachs
W, et al. Extreme diversity of tropical parasitoid wasps exposed by itera-
tive integration of natural history, DNA barcoding, morphology, and
collections. Proc Natl Acad Sci. 2008;105:12359–64.
80. Condon MA, Scheffer SJ, Lewis ML, Wharton R, Adams DC, Forbes AA.
Lethal interactions between parasites and prey increase niche diversity
in a tropical community. Science. 2014;343:1240–4.
81. Forbes AA, Devine SN, Hippee AC, Tvedte ES, Ward AKG, Widmayer
HA, et al. Revisiting the particular role of host shifts in initiating insect
speciation. Evolution. 2017;71:1126–37.
82. Stehr FW, Cook EF. A revision of the genus Malacosoma Hübner in
North America (Lepidoptera: Lasiocampidae): systematics, biology,
immatures, and parasites. Washington, D.C.: Smithsonian Institution
Press; 1968.
83. Powell THQ, Forbes AA, Hood GR, Feder JL. Ecological adaptation
and reproductive isolation in sympatry: genetic and phenotypic
evidence for native host races of Rhagoletis pomonella. Mol Ecol.
2014;23:688–704.
84. Bagley RK, Sousa VC, Niemiller ML, Linnen CR. History, geography
and host use shape genomewide patterns of genetic variation in the
redheaded pine sawfly (Neodiprion lecontei). Mol Ecol. 2017;26:1022–44.
85. Hood GR, Forbes AA, Powell THQ, Egan SP, Hamerlinck G, Smith JJ, et al.
Sequential divergence and the multiplicative origin of community
diversity. Proc Natl Acad Sci. 2015;112:E5980–9.
86. Juliano SA. Trichogramma spp. (Hymenoptera: Trichogrammatidae) as
egg parasitoids of Sepedon fuscipennis (Diptera: Sciomyzidae) and other
aquatic Diptera. Can Entomol. 1981;113:271–9.
87. Elliott JM. The life cycle and spatial distribution of the aquatic parasitoid
Agriotypus armatus (Hymenoptera: Agriotypidae) and its caddis host
Silo pallipes (Trichoptera: Goeridae). J Anim Ecol. 1982;51:923–41.
88. Fernandez-Triana J, Smith MA, Boudreault C, Goulet H, Hebert PDN,
Smith AC, et al. A poorly known high-latitude parasitoid wasp commu-
nity: unexpected diversity and dramatic changes through time. PLoS
ONE. 2011;6:e23719.
89. Lasalle J. North American genera of Tetrastichinae (Hymenoptera:
Eulophidae). J Nat Hist. 1994;28:109–236.
90. Finch OD. The parasitoid complex and parasitoid-induced mortal-
ity of spiders (Araneae) in a Central European woodland. J Nat Hist.
2005;39:2339–54.
91. Stahlhut JK, Fernández-Triana J, Adamowicz SJ, Buck M, Goulet H,
Hebert PD, et al. DNA barcoding reveals diversity of Hymenoptera and
the dominance of parasitoids in a sub-arctic environment. BMC Ecol.
2013;13:2.
92. Kimsey L, Zavortink T, Kimsey R, Heydon S. Insect biodiversity of the
Algodones Dunes of California. Biodivers Data J. 2017;5:e21715.
93. Hebert PDN, Ratnasingham S, Zakharov EV, Telfer AC, Levesque-Beaudin
V, Milton MA, et al. Counting animal species with DNA barcodes: cana-
dian insects. Philos Trans R Soc B Biol Sci. 2016;371:20150333.
94. Borkent A, Brown BV, Adler PH, de Amorim DS, Barber K, Bickel D, et al.
Remarkable fly (Diptera) diversity in a patch of Costa Rican cloud forest:
why inventory is a vital science. Zootaxa. 2018;4402:53–90.
95. Brown BV, Borkent A, Adler PH, de Amorim DS, Barber K, Bickel D, et al.
Comprehensive inventory of true flies (Diptera) at a tropical site. Com-
mun Biol. 2018;1:21.
96. Veijalainen A, Wahlberg N, Broad GR, Erwin TL, Longino JT, Saaksjarvi
IE. Unprecedented ichneumonid parasitoid wasp diversity in tropical
forests. Proc R Soc B Biol Sci. 2012;279:4694–8.
97. Eagalle T, Smith MA. Diversity of parasitoid and parasitic wasps across
a latitudinal gradient: using public DNA records to work within a taxo-
nomic impediment. FACETS. 2017;2:937–54.
98. Gómez IC, Sääksjärvi IE, Mayhew PJ, Pollet M, Rey del Castillo C, Nieves-
Aldrey JL, et al. Variation in the species richness of parasitoid wasps
(Ichneumonidae: Pimplinae and Rhyssinae) across sites on different
continents. Insect Conserv Divers. 2017;11:305–16.
99. Grucmanová Ŝ, Holuša J. Nematodes associated with bark beetles, with
focus on the genus Ips (Coleoptera: Scolytinae) in Central Europe. Acta
Zool Bulg. 2013;65:547–56.
100. Walter DE, Proctor HC. Mites: ecology, evolution & behaviour: life at a
microscale. 2nd ed. Dordrecht: Springer; 2013.
... Surprisingly, however, in the most speciose animal class, the insects, that are already known to have descending pathways for non-nociceptive behaviours (e.g. locomotion [11,12] and sexual behaviour [13,14]), such descending pain controls have been little investigated [15,16]. ...
... Further, insect nociceptive processing can be modulated (e.g. [15,16]). For example, the tobacco hornworm (Manduca sexta) shows a defensive nociceptive behaviour in response to a noxious pinch, performing a rapid bending response toward the pinch site (figure 1), and this response can be sensitized by tissue damage [19,20]. ...
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Modulation of nociception allows animals to optimize chances of survival by adapting their behaviour in different contexts. In mammals, this is executed by neurons from the brain and is referred to as the descending control of nociception. Whether insects have such control, or the neural circuits allowing it, has rarely been explored. Based on behavioural, neuroscientific and molecular evidence, we argue that insects probably have descending controls for nociception. Behavioural work shows that insects can modulate nocifensive behaviour. Such modulation is at least in part controlled by the central nervous system since the information mediating such prioritization is processed by the brain. Central nervous system control of nociception is further supported by neuroanatomical and neurobiological evidence showing that the insect brain can facilitate or suppress nocifensive behaviour, and by molecular studies revealing pathways involved in the inhibition of nocifensive behaviour both peripherally and centrally. Insects lack the endogenous opioid peptides and their receptors that contribute to mammalian descending nociception controls, so we discuss likely alternative molecular mechanisms for the insect descending nociception controls. We discuss what the existence of descending control of nociception in insects may reveal about pain perception in insects and finally consider the ethical implications of these novel findings.
... 1. When the extant taxa are constrained to match molecular phylogenetic topologies, that is, Polyphaga (Adephaga (Myxophaga, Archostemata)) (Figure 2c), seven states are implausibly reversed (Bergsten et al., 2013; Beutel, 1997; Escalona et al., 2020;Forbes, 1928;Forbes et al., 2018;Haas, 1998;He et al., 2015;Hörnschemeyer et al., 2002). This would require for the ancestor of the Archostemata the re-evolution or loss of specific features from several anatomical systems that are preserved in the Palaeozoic fossil record, namely: regain of cuticular sculpture and tubercle specification (C3, 4), loss or reduction of the prosternal process (C22), regain of the transverse ridge of the mesoventrite (C29), regain of highly reticulate crossveins of deep relief (C33), and reexposure of the metatrochantin (C39). ...
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The Coleoptera provides an excellent example of the value of fossils for understanding the evolutionary patterns of recent lineages. We reevaluate the morphology of the Early Perm-ian †Tshekardocoleidae to test alternative phylogenetic hypotheses relating to the Palaeozoic evolution of the order. We discuss prior interpretations and revise an earlier data matrix. Both Bayesian and parsimony analyses support the monophyly of Coleoptera excluding †Tshekardocoleidae (= Mesocoleoptera), and of Coleoptera excluding †Tshekardocoleidae and †Permocupedidae (= Metacoleoptera). Plesiomorphies preserved in †Tshekardocoleidae are elytra, which rest over the body in a loose tent-like manner, with flat lateral flanges, projecting beyond the abdominal apex, and abdomens that are flexible and nearly cylindrical. Apomorphies of Mesocoleoptera include shortening of the elytra and a closer fit with the flattened and probably more rigid abdomen. A crucial synapomorphy of Metacoleoptera is the tightly sealed subelytral space, which may have been advantageous during the Permian aridification. Taxon exclusion experiments show that †Tshekardocoleidae is crucial for understanding the early evolution of Coleoptera and that its omission strongly affects ancestral state polarities as well as topology, including crown-group taxa. By constraining the relationships of extant taxa to match those supported by phylogenomic analysis, we demonstrate that features shared by Archostemata with Permian stem groups are most reasonably supported as plesiomorphic and that the smooth and simplified body forms of Polyphaga, Adephaga, Myxophaga, and Micromalthidae were derived in parallel. Our study highlights the reciprocal illumination of molecular, morphological, and paleontological data, and paves the way for tip-dating analysis across the order.
... Therefore, alteration of herbivore behaviour or saliva composition could, in turn, alter herbivore-induced plant responses. Such herbivore alteration typically happens when herbivores are parasitised by parasitic wasps (also called 'parasitoids') that attack herbivorous insects (Forbes et al., 2018;Vinson & Iwantsch, 1980). Parasitoids typically lay one (solitary) or several (gregarious) eggs in their herbivorous host which can often still feed on plants during the parasitoid larval development (koinobiont parasitoids) (Godfray, 1994). ...
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1. Upon parasitism, many parasitoids inject symbiotic viruses and venom into their host. Thereby, they modify the hosts physiology including its saliva composition and, in turn, plant perception of herbivory. 2. It has been hypothesised that parasitoids manipulate plant responses to increase their host performance and maximise their own fitness. However, it is still unclear whether parasitoids are under selective pressure to increase plant quality or whether indirect changes in plants due to parasitism are a by-product of the physiological changes induced in their host. 3. We tested whether the parasitoids Hyposoter ebeninus and Cotesia glomerata manipulate induced plant responses through the host Pieris brassicae caterpillars to increase their own performance. During their entire lifespan, parasitised herbivores were fed with leaf material of Brassica oleracea plants that were left untreated or continuously exposed to feeding by either unparasitised, conspecific or heterospe-cific parasitised caterpillars. We measured the development time, weight, clutch size and mortality of parasitoids that emerged from caterpillars as proxy for their performance. 4. Both parasitoid species did not perform significantly better when their host was fed with leaves from plants continuously induced by a conspecific parasitoid relative to unparasitised caterpillars. However, parasitoid species asymmetrically affected each other's performance through plant-mediated interactions. 5. Our results do not support the hypothesis of parasitoids manipulating plant responses for their own benefit, suggesting that indirect plant-mediated interactions among parasitoids may be a by-product of host manipulation. However, our work confirms the significance of parasitoid-induced plant-mediated interactions in insect communities that to date are still understudied.
... Colombia tiene una posición geográfica, una complejidad vegetal y una diversidad de ecosistemas que lo convierten en un país verdaderamente privilegiado en biodiversidad, lo que le ha permitido ocupar primeros lugares a nivel mundial en varios grupos, como el tercero en diversidad de mariposas diurnas con más de 3.780 especies, distribuidas en las familias Hesperiidae, Papilionidae, Pieridae, Nymphalidae, Riodinidae y Lycaenidae (FORBES et al., 2018;HUERTAS & ARIAS 2007;LAMAS, 2004). En el departamento de Santander su estudio se ha limitado a capturas en el marco de proyectos de caracterización de flora y fauna silvestre, salidas y prácticas docentes, trabajos de grado y consultorías ambientales, lo cual ha suministrado abundantes datos sobre la fauna local, aunque todavía quedan zonas del nororiente colombiano por ser estudiadas, y que indudablemente tiene mucho por decir en términos biológicos y medioambientales (CASAS et al., 2017;HUERTAS & ARIAS, 2007;VILLALOBOS-MORENO, 2013VILLALOBOS-MORENO & GÓMEZ, 2015VILLALOBOS-MORENO & SALAZAR-ESCOBAR, 2020aVILLALOBOS-MORENO et al., 2012. ...
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Se realizaron capturas de los Lepidoptera diurnas dentro del proyecto de “Caracterización de la Entomofauna silvestre de la cuenca de río Cachirí, jurisdicción de la CDMB”, la cual se ubica en el departamento de Santander, al nororiente de los Andes colombianos, en bosques secundarios en un gradiente altitudinal entre los 400 y 3.250 msnm, con el propósito de establecer una línea base sobre la diversidad entomológica, y eventualmente detectar ele�mentos faunísticos para la conservación de zonas boscosas dentro de la cuenca. Se colectaron 331 ejemplares de 112 especies pertenecientes a las familias Hesperiidae, Papilionidae, Pieridae, Lycaenidae, Riodinidae y Nymphalidae. La familia Nymphalidae fue la mayor abundancia (191) y riqueza de especies (66). Santa Rosa (1.220 msnm) fue el sitio con mayor abundancia (91) y mayor riqueza de especies (47). El análisis de la calidad del inventario indicó una riqueza potencial de especies de 224,35, una proporción de especies observadas del 49,92% y un esfuerzo de mues�treo del 99,78%. Santa Rosa fue la localidad con los mayores valores de diversidad: abundancia (91), riqueza obser�vada (47), riqueza potencial (115,17), diversidad de orden 1 (38,84) y diversidad de orden 2 (31,73). La compara�ción de los inventarios de los sitios de muestreo permitió determinar que no existe similitud entre estas localidades, lo cual se puede explicar por las distancias altitudinales y geográficas entre ellas. PALABRAS CLAVE: Lepidoptera, Papilionoidea, abundancia, Andes colombianos, diversidad, riqueza de especies, Colombia.
... Colombia tiene una posición geográfica, una complejidad vegetal y una diversidad de ecosistemas que lo convierten en un país verdaderamente privilegiado en biodiversidad, lo que le ha permitido ocupar primeros lugares a nivel mundial en varios grupos, como el tercero en diversidad de mariposas diurnas con más de 3.780 especies, distribuidas en las familias Hesperiidae, Papilionidae, Pieridae, Nymphalidae, Riodinidae y Lycaenidae (FORBES et al., 2018;HUERTAS & ARIAS 2007;LAMAS, 2004). En el departamento de Santander su estudio se ha limitado a capturas en el marco de proyectos de caracterización de flora y fauna silvestre, salidas y prácticas docentes, trabajos de grado y consultorías ambientales, lo cual ha suministrado abundantes datos sobre la fauna local, aunque todavía quedan zonas del nororiente colombiano por ser estudiadas, y que indudablemente tiene mucho por decir en términos biológicos y medioambientales (CASAS et al., 2017;HUERTAS & ARIAS, 2007;VILLALOBOS-MORENO, 2013VILLALOBOS-MORENO & GÓMEZ, 2015VILLALOBOS-MORENO & SALAZAR-ESCOBAR, 2020aVILLALOBOS-MORENO et al., 2012. ...
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Resumen Se realizaron capturas de los Lepidoptera diurnas dentro del proyecto de "Caracterización de la Entomofauna silvestre de la cuenca de río Cachirí, jurisdicción de la CDMB", la cual se ubica en el departamento de Santander, al nororiente de los Andes colombianos, en bosques secundarios en un gradiente altitudinal entre los 400 y 3.250 msnm, con el propósito de establecer una línea base sobre la diversidad entomológica, y eventualmente detectar elementos faunísticos para la conservación de zonas boscosas dentro de la cuenca. Se colectaron 331 ejemplares de 112 especies pertenecientes a las familias Hesperiidae, Papilionidae, Pieridae, Lycaenidae, Riodinidae y Nymphalidae. La familia Nymphalidae fue la mayor abundancia (191) y riqueza de especies (66). Santa Rosa (1.220 msnm) fue el sitio con mayor abundancia (91) y mayor riqueza de especies (47). El análisis de la calidad del inventario indicó una riqueza potencial de especies de 224,35, una proporción de especies observadas del 49,92% y un esfuerzo de muestreo del 99,78%. Santa Rosa fue la localidad con los mayores valores de diversidad: abundancia (91), riqueza observada (47), riqueza potencial (115,17), diversidad de orden 1 (38,84) y diversidad de orden 2 (31,73). La comparación de los inventarios de los sitios de muestreo permitió determinar que no existe similitud entre estas localidades, lo cual se puede explicar por las distancias altitudinales y geográficas entre ellas.
... Because DNA evidence places our specimens within Centistes the differences seen in mandible size may represent derived traits not previously noted for Centistes. Such a gap in knowledge would not be unexpected given that the variability of cephalic structures in North American Centistes larvae has probably not been fully documented (Forbes et al. 2018) and thus the range of mandible morphology is not known. In addition to morphology, the fact that our specimens were koinobiont endoparasitoids from chrysomelid beetles further confirms their membership in Euporhinae and Centistini given that this combination of traits are essentially unique to these groups ( van Achterberg 1976;Quicke and van Achterberg 1990;Quicke 2015). ...
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Globalized trade has resulted in the incidental translocation of numerous insect species, some of which have become invasive in their expanded ranges. While rigorous inspection programs are a regular part of commodity importation, rarely if ever are the internal contents of intercepted insects examined. As part of a genetic diversity project on intercepted Diabrotica undecimpunctata beetles, we detected CO1 DNA that closely matched sequences from Centistes parasitoid wasps in 9% of our samples. The presence of internal parasitoids was confirmed through dissections and imaging, wherein the samples were morphologically consistent with Centistes larvae. Such a discovery suggests that insect translocation as part of trade can be more diverse than initially thought. The case of Centistes in imported Diabrotica may present a positive benefit specifically to agroecosystems through the biological control of pest beetles like Diabrotica. However , drawbacks from such introductions include off-target parasitism of non-pest beetles and resultant impacts to insect populations in undisturbed ecosystems. Thus, examination of intercepted insects beyond the initial species identification is warranted to better understand the potential impacts of human mediated insect translocations. Methods employing high-throughput sequencing and metabarcoding are well suited for such broad-scale identification projects where Diabrotica would be an excellent candidate for this work.
... Hymenopteran parasitoids are probably one of the most diverse groups of animals (Forbes et al., 2018), yet much of their biology and ecology remains unknown due to their small size and often problematic taxonomy. We used an integrative approach to identify 35 ...
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Cryptic species diversity is a major challenge for the species-rich community of parasitoids attacking oak gall wasps due to a high degree of sexual dimorphism, morphological plasticity, small size, and poorly known biology. As such, we know very little about the number of species present, nor the evolutionary forces responsible for generating this diversity. One hypothesis is that trait diversity in the gall wasps, including the morphology of the galls they induce, has evolved in response to selection imposed by the parasitoid community, with reciprocal selection driving diversification of the parasitoids. Using a rare, continental-scale data set of Sycophila parasitoid wasps reared from 44 species of cynipid galls from 18 species of oak across the US, we combined mitochondrial DNA barcodes, Ultraconserved Elements (UCEs), morphological, and natural history data to delimit putative species. Using these results, we generate the first large-scale assessment of ecological specialization and host association in this species-rich group, with implications for evolutionary ecology and biocontrol. We find most Sycophila target specific subsets of available cynipid host galls with similar morphologies, and generally attack larger galls. Our results suggest that parasitoid wasps such as Sycophila have adaptations allowing them to exploit particular host trait combinations, while hosts with contrasting traits are resistant to attack. These findings support the tritrophic niche concept for the structuring of plant-herbivore-parasitoid communities.
... Unfortunately, these models may not be entirely appropriate null predictions for most arrhenotokous animals because of confounding sex-specific expression. All Hymenoptera-potentially the most speciose order of insects (Forbes et al. 2018)-are arrhenotokous. Unfertilized hymenopteran eggs develop into males, and fertilized eggs usually develop into females (Harpur et al. 2013;Slater et al. 2020). ...
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Many species have separate haploid and diploid phases. Theory predicts that each phase should experience the effects of evolutionary forces (like selection) differently. In the haploid phase, all fitness-affecting alleles are exposed to selection, whereas in the diploid phase, those same alleles can be masked by homologous alleles. This predicts that selection acting on genes expressed in haploids should be more effective than diploid-biased genes. Unfortunately, in arrhenotokous species, this prediction can be confounded with the effects of sex-specific expression, as haploids are usually reproductive males. Theory posits that, when accounting for ploidal- and sex-specific expression, selection should be equally efficient on haploid- and diploid-biased genes relative to constitutive genes. Here, we used a multiomic approach in honey bees to quantify the evolutionary rates of haploid-biased genes and test the relative effects of sexual- and haploid-expression on molecular evolution. We found that 16% of the honey bee's protein-coding genome is highly expressed in haploid tissue. When accounting for ploidy and sex, haploid- and diploid-biased genes evolve at a lower rate than expected, indicating that they experience strong negative selection. However, the rate of molecular evolution of haploid-biased genes was higher than diploid-based genes. Genes associated with sperm storage are a clear exception to this trend with evidence of strong positive selection. Our results provide an important empirical test of theory outlining how selection acts on genes expressed in arrhenotokous species. We propose the haploid life history stage affects genome-wide patterns of diversity and divergence because of both sexual and haploid selection.
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In the lengthy co-evolution between insects and their animal or plant hosts, insects have evolved a wide range of salivary strategies to help evade host defenses. Although there is a very large literature on saliva of herbivorous and hematophagous insects, little attention has been focused on the saliva of parasitoid wasps. Some parasitoid species are natural enemies that effectively regulate insect population sizes in nature that they are applied for biological control of agricultural pests. Here, we demonstrate the influence of the endoparasitoid, Pteromalus puparum, larval saliva on the cellular and humoral immunity of its host. Larval saliva increases mortality of hemocytes, and inhibits hemocyte spreading, a specific cellular immune action. We report that high saliva concentrations inhibit host cellular encapsulation of foreign invaders. The larval saliva also inhibits melanization in host hemolymph. The saliva inhibits the growth of some bacterial species, Bacillus subtilis, Staphylococcus aureus and Pseudomonas aeruginosa in vitro. This may promote larvae fitness by protecting them from infections. Insight into such functions of parasitic wasp saliva provides a new insight into host-parasitoid relationships and possibly leads to new agricultural pest management technologies.
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1 Many species have separate haploid and diploid phases. Theory predicts that each phase should 2 experience the effects of evolutionary forces (like selection) differently. In the haploid phase, all fitness-3 affecting alleles are exposed to selection whereas in the diploid phase those same alleles can be masked 4 by homologous alleles. This predicts that selection acting on genes expressed in haploids should be more 5 effective than diploid-biased genes. Unfortunately, in arrhenotokous species this prediction can be 6 confounded with the effects of sex-specific expression, as haploids are usually reproductive males. 7 Theory posits that, when accounting for ploidal-and sex-specific-expression, selection should be equally 8 efficient on haploid-and diploid-biased genes relative to constitutive genes. Here, we used a multi-omic 9 approach in honey bees to quantify the evolutionary rates of haploid-biased genes and test the relative 10 effects of sexual-and haploid-expression on molecular evolution. We found that 16% of the honey bee's 11 protein-coding genome is highly expressed in haploid tissue. When accounting for ploidy and sex, 12 haploid-and diploid-biased genes evolve at a lower rate than expected, indicating that they experience 13 strong negative selection. However, the rate of molecular evolution of haploid-biased genes was higher 14 than diploid-based genes. Genes associated with sperm storage are a clear exception to this trend with 15 evidence of strong positive selection. Our results provide an important empirical test of theory outlining 16 how selection acts on genes expressed in arrhenotokous species. We propose the haploid life history stage 17 affects genome-wide patterns of diversity and divergence because of both sexual and haploid selection. 18 A common feature of most eukaryotic species is the presence of a separate haploid and diploid phase. 22 Theory predicts that each phase should experience the effects of natural selection and drift differently. In 23 a haploid phase, for example, all deleterious alleles are exposed to selection whereas in diploid phases 24 those same alleles can be masked by homologous alleles. Unfortunately, for haplodiploid animal species, 25 this prediction can be confounded with sexual selection as haploids are usually reproductive males. Here, 26 we develop theory to predict how haploid-and sex-specific genes should evolve. We then use honey bees 27 as a model to empirically test our predictions. We found that at least 16% of the honey bee's protein-28 coding genome is highly expressed in haploid tissue. When accounting for ploidy and sex, there are 29 significant differences in the molecular rates of evolution of haploid-biased genes relative to other 30 diploid-biased and constitutively expressed genes sets. Despite this, haploid-biased genes tend to have 31 much lower evolutionary rates than predicted. However, haploid-biased sperm storage genes are an 32 exception. Our results provide an important empirical test of theory outlining how selection acts on genes 33 expressed in arrhenotokous species. We propose the haploid life-history stage affects genome-wide 34 patterns of diversity and divergence because of both sexual and haploid selection.
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Estimations of tropical insect diversity generally suffer from lack of known groups or faunas against which extrapolations can be made, and have seriously underestimated the diversity of some taxa. Here we report the intensive inventory of a four-hectare tropical cloud forest in Costa Rica for one year, which yielded 4332 species of Diptera, providing the first verifiable basis for diversity of a major group of insects at a single site in the tropics. In total 73 families were present, all of which were studied to the species level, providing potentially complete coverage of all families of the order likely to be present at the site. Even so, extrapolations based on our data indicate that with further sampling, the actual total for the site could be closer to 8000 species. Efforts to completely sample a site, although resource-intensive and time-consuming, are needed to better ground estimations of world biodiversity based on limited sampling.
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Study of all flies (Diptera) collected for one year from a four-hectare (150 x 266 meter) patch of cloud forest at 1,600 meters above sea level at Zurquí de Moravia, San José Province, Costa Rica (hereafter referred to as Zurquí), revealed an astounding 4,332 species. This amounts to more than half the number of named species of flies for all of Central America. Specimens were collected with two Malaise traps running continuously and with a wide array of supplementary collecting methods for three days of each month. All morphospecies from all 73 families recorded were fully curated by technicians before submission to an international team of 59 taxonomic experts for identification. Overall, a Malaise trap on the forest edge captured 1,988 species or 51% of all collected dipteran taxa (other than of Phoridae, subsampled only from this and one other Malaise trap). A Malaise trap in the forest sampled 906 species. Of other sampling methods, the combination of four other Malaise traps and an intercept trap, aerial/hand collecting, 10 emergence traps, and four CDC light traps added the greatest number of species to our inventory. This complement of sampling methods was an effective combination for retrieving substantial numbers of species of Diptera. Comparison of select sampling methods (considering 3,487 species of non-phorid Diptera) provided further details regarding how many species were sampled by various methods. Comparison of species numbers from each of two permanent Malaise traps from Zurquí with those of single Malaise traps at each of Tapantí and Las Alturas, 40 and 180 km distant from Zurquí respectively, suggested significant species turnover. Comparison of the greater number of species collected in all traps from Zurquí did not markedly change the degree of similarity between the three sites, although the actual number of species shared did increase. Comparisons of the total number of named and unnamed species of Diptera from four hectares at Zurquí is equivalent to 51% of all flies named from Central America, greater than all the named fly fauna of Colombia, equivalent to 14% of named Neotropical species and equal to about 2.7% of all named Diptera worldwide. Clearly the number of species of Diptera in tropical regions has been severely underestimated and the actual number may surpass the number of species of Coleoptera. Various published extrapolations from limited data to estimate total numbers of species of larger taxonomic categories (e.g., Hexapoda, Arthropoda, Eukaryota, etc.) are highly questionable, and certainly will remain uncertain until we have more exhaustive surveys of all and diverse taxa (like Diptera) from multiple tropical sites. Morphological characterization of species in inventories provides identifications placed in the context of taxonomy, phylogeny, form, and ecology. DNA barcoding species is a valuable tool to estimate species numbers but used alone fails to provide a broader context for the species identified.
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Estimations of tropical insect diversity generally suffer from lack of known groups or faunas against which extrapolations can be made, and have seriously underestimated the diversity of some taxa. Here we report the intensive inventory of a four-hectare tropical cloud forest in Costa Rica for one year, which yielded 4332 species of Diptera, providing the first verifiable basis for diversity of a major group of insects at a single site in the tropics. In total 73 families were present, all of which were studied to the species level, providing potentially complete coverage of all families of the order likely to be present at the site. Even so, extrapolations based on our data indicate that with further sampling, the actual total for the site could be closer to 8000 species. Efforts to completely sample a site, although resource-intensive and time-consuming, are needed to better ground estimations of world biodiversity based on limited sampling.
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Beetles (Coleoptera) are the most diverse and species-rich group of insects, and a robust, time-calibrated phylogeny is fundamental to understanding macroevolutionary processes that underlie their diversity. Here we infer the phylogeny and divergence times of all major lineages of Coleoptera by analyzing 95 protein-coding genes in 373 beetle species, including ~67% of the currently recognized families. The subordinal relationships are strongly supported as Polyphaga (Adephaga (Archostemata, Myxophaga)). The series and superfamilies of Polyphaga are mostly monophyletic. The species-poor Nosodendridae is robustly recovered in a novel position sister to Staphyliniformia, Bostrichiformia, and Cucujiformia. Our divergence time analyses suggest that the crown group of extant beetles occurred ~297 million years ago (Mya) and that ~64% of families originated in the Cretaceous. Most of the herbivorous families experienced a significant increase in diversification rate during the Cretaceous, thus suggesting that the rise of angiosperms in the Cretaceous may have been an 'evolutionary impetus' driving the hyperdiversity of herbivorous beetles.
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1. The old idea that parasitoid wasps (Ichneumonidae) show an inverse latitudinal diversity gradient has recently been challenged, but how ichneumonid species richness varies across the globe is still not well understood. We carried out field inventories in 21 sites on three continents to clarify this question, focusing on the subfamilies Pimplinae and Rhyssinae. Our total sampling effort was 628 Malaise trap months and the total catch exceeded 65 000 individuals. Our main focus was in two intensively inventoried areas in Amazonia, together yielding 257 Malaise trap months and 26 390 ichneumonid individuals. 2. To expand the scope and assess global species diversity patterns of the Pimplinae and Rhyssinae, we compiled published species lists from a total of 97 study localities around the world. The highest observed species richness in any locality, 105 species, was found in one of our field sites in Peruvian Amazonia. None of the other localities reported more than 70 species, even the ones with a sampling effort comparable to ours. 3. Despite the local thoroughness of our field inventories in Amazonia, data analyses indicated that a substantial proportion of the parasitoid wasp species occurring in each site remained unobserved. 4. The highest local species richness values were reported from the tropics. Nevertheless parasitoid wasps are still too sparsely sampled to draw solid conclusions about whether or not their species richness follows a particular latitudinal trend, and if so, where their richness peaks.
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Divergent host use has long been suspected to drive population differentiation and speciation in plant-feeding insects. Evaluating the contribution of divergent host use to genetic differentiation can be difficult, however, as dispersal limitation and population structure may also influence patterns of genetic variation. In this study, we use double-digest restriction-associated DNA (ddRAD) sequencing to test the hypothesis that divergent host use contributes to genetic differentiation among populations of the redheaded pine sawfly (Neodiprion lecontei), a widespread pest that uses multiple Pinus hosts throughout its range in eastern North America. Because this species has a broad range and specializes on host plants known to have migrated extensively during the Pleistocene, we first assess overall genetic structure using model-based and model-free clustering methods, and identify three geographically distinct genetic clusters. Next, using a composite-likelihood approach based on the site frequency spectrum and a novel strategy for maximizing the utility of linked RAD markers, we infer the population topology and date divergence to the Pleistocene. Based on existing knowledge of Pinus refugia, estimated demographic parameters, and patterns of diversity among sawfly populations, we propose a Pleistocene divergence scenario for N. lecontei. Finally, using Mantel and partial Mantel tests, we identify a significant relationship between genetic distance and geography in all clusters, and between genetic distance and host use in two of three clusters. Overall, our results indicate that Pleistocene isolation, dispersal limitation, and ecological divergence all contribute to genome-wide differentiation in this species, and support the hypothesis that host use is a common driver of population divergence in host-specialized insects. This article is protected by copyright. All rights reserved.