How
Quıckly
Do Insects Evolve?
K.G. ANDREW HAMILTON
T
he length of time required by evolution to produce
a new terrestrial species is usually measured by
fossil data from marine environments and land
vertebrates. These suggest that evolution is more than
glacially slow, proceeding incrementally over millions
of years; but on the other hand, there are 300 species
of closely related cichlid fish in Lake Victoria, a body of
water that is less than a million years old; and possibly
all those species evolved as little as 12,000 years ago
when the lake was most recently dry (Wilkins 2013).
Data on the rate of insect speciation is much sparser.
This is partly because fossil insects are seldom preserved
with sufficient detail to allow analysis of inter-species
divergences, and partly because modern insects disperse
14
so rapidly and easily, even across large bodies of water,
that their evolution can be correlated only rarely with
geological features of known age. The best situations
for linking arthropod evolution to geological events are
caves (Caccone and Sbordoni 2001) and the Hawaiian
Islands (Gillespie 2005, Rubinoff unpublished).
It was therefore exciting to become involved in
a taxonomic study of the first such study of insects
widespread on a continental landscape. The leafhoppers of the genus Errhomus Oman (Hemiptera:
Cicadellidae), like their relatives, always have flightless
females (Oman and Musgrave 1975). These and other
leafhoppers were neither displaced nor eradicated by
Pleistocene glaciation, leaving a rich endemic fauna
American Entomologist • Spring 2014
across the Great Plains and arid parts of the cordilleran
system as far north as Washington state and western
Montana (Hamilton 2002). Their numerous species
and subspecies (Oman 1987) are separated by deeply
dissected lava plains from Washington state to southern Idaho that were left in the wake of the geological
“hot spot” now located under Yellowstone National
Park (Leeman et al. 2008). Rivers have cut through
the soft basaltic rocks, creating the enormously deep
canyons of the Columbia Basin (Fig. 1, heavy black
Fig. 1. The leafhopper genus Errhomus (insert) and its distribution around lava fields and across canyons (black) in the Pacific
Northwest, from British Columbia (BC) to Colorado (CO). Yellow
areas indicate the range of a few widely distributed species (E.
calvus, E. lineatus, E. similis including subspecies medialis, and
E. variabilis); red and small numbers indicate the nominate
subgenus (1, E. picturatus; 2, E. wolfei; 3, E. reflexus; 4, E. satus;
5, E. ochoco; 6, E. paradoxus; 7, E. winquatt; 8, E. brevis; 9, E.
josephi); larger numbers represent the more widely dispersed
subgenus Erronus: yellow spots marked 1, the widespread E.
montanus in MT to CO; blue spots represent highly localized
but widely scattered species marked 2 (E. solus in MT), 3 (E.
instabilis in WA), 4-6 (E. camensis, E. rivalis and E. bracatus in
MT), 7 (E. naomi in UT), and 8-10 (E. affinis, E. serratus, and
E. pallidus bordering Hell’s Canyon). Lava fields are indicated
by age in grey (WA, 18 my BP), lilac (ID, 12 my BP) and pink
(WY, recent). Photos by Tom Murray and by Joanne Elsaesser.
lines) in the Pacific Northwestern states and adjacent
Canada. The most recent canyon (Hell’s Canyon on
the Washington-Idaho border) is considered to be 1.6
million years old, and the lower Columbia gorge very
much older, at 12 million years (Waitt and Swanson
1987). Each of these canyons has sister-taxa of Errhomus on either side (Hamilton and Zack 1999). A phylogeny derived from unique morphological evidence
coupled with geological evidence of huge lava flows
and subsequent canyon formation suggested massive
extinction early in the evolution of the genus followed
by episodic speciation as the plateau became dissected by rivers (Fig. 2). There was, however, no concrete
evidence that the species in question were that old,
and analysis of the female characters suggests ongoing introgression, presumably by males blown across
the river valleys. Could genetic evidence decisively
test these hypotheses?
Genetic Analysis
This project analyzes “barcoding” DNA (utilizing a
658-base-pair segment of the COI gene) that can
characterize specimens collected over the previous
60 years and can compare them using neighbor-joining
algorithms (Fig. 3). Such genetic analysis measures the
divergence of maternally inherited mitochondrial DNA
only, thus eliminating possible introgression factors
from hybridism and making it possible to track the
spread of flightless females such as those of Errhomus.
In groups like the Hemiptera in which nymphs may or
may not resemble adults, it also makes possible the integration of nymphal taxonomic characters and a fuller
appreciation of the nature of genera. Sequences, trace
files, collection data, and specimen photographs are
deposited in the Barcode of Life Datasystem (BOLD).
In a pilot study, 1,150 specimens of Hemiptera-Auchenorrhyncha representing 471 species from the Canadian National Collection of Insects were successfully
tested. These were mostly large specimens of spittlebugs (Cercopoidea), cicadas (Cicadoidea), planthoppers
Fig. 2. Phylogeny of Errhomus based on “barcode” genetic analysis, showing concordance of genetic divergence and age of lineages, with absolute time scale determined by five major geological events, listed in upper left.
16
(Fulgoroidea), and treehoppers as well as leafhoppers
(Membracoidea). Subsequently, an additional 2,400 specimens of smaller leafhoppers and planthoppers also were
barcoded in an attempt to include as many as possible
of the nearctic genera and their relatives. An average of
2.5 specimens per species was used to cover geographic
variation and to test for uniformity within series taken at
the same time on the same host. Initial trials indicated
that the probability of a successful genetic analysis diminishes beyond 30 years, so more specimens were used if
the only specimens available were collected before 1980.
The first iterations compared 22 species of Errhomus
(from specimens collected after Oman’s 1987 study) to
those of other genera; the last iteration incorporated
the 24 subspecies and various local hybrid populations.
Very minor differences were found when additional
data were incorporated to such a large data set, and
the whole resulting phylogeny differed very little from
the morphologically derived phylogeny (Hamilton and
Zack 1999, Fig. 90). One subspecies (obliteratus) was
found to be associated with the wrong adjacent species;
another putative subspecies (instabilis) is probably a
valid species, being widely divergent genetically and
also geographically isolated from its nearest relative;
and two putative species (ochoco and paradoxus) are
probably subspecies of their closest relatives (ochoco
is an isolated population at Mt. Ochoco summit pass,
and paradoxus lies on the far side of a shallow part of
the Columbia River, where a crossing by way of former
oxbows might have been possible).
Similar instances in other genera of congruence
between genetic and morphological data were common
in this analysis. Most leafhopper genera were verified,
both those with numerous species and also many small
genera, although those with fewest species usually barcode as autapomorphic subgenera. In two cases, there
were sufficient species successfully barcoded to verify
published phylogenies, but both these genera lack the
geographic evidence that forms a significant part of the
phylogenetic analysis in Errhomus and the fit between
morphological and genetic data is not as consistent.
A morphological analysis of the large, holarctic leafhopper genus Limotettix Sahlberg grouped four former
genera and a new, basal subgenus (Hamilton 1994,
McKamey 2001) based on a single unique morphological character. That analysis corresponds well with
barcode data on 46 nearctic species, grouping all these
taxa in the same manner, although not necessarily in
the same sequence where unique morphological characters were lacking.
More significantly, a phylogeny utilizing both morphological and genetic data of the 44 species of the
grass-feeding genus Flexamia DeLong (Whitcomb and
Hicks 1988) was supported by parsimony analysis of
whole-gene mitochondrial DNA (Dietrich et al. 1997)
and now by neighbor-joining analysis of barcode data
in 35 species, including one that is new to science. Each
analysis recovers the same species groups, but they all
differ in some arrangement of individual species. Recovery of the species groups is critically important in this
American Entomologist • Spring 2014
genus, as each species group feeds on a different host
genus, implying stable ecological relationships with
prairie habitats over millions of years (Hamilton 2006).
However, as in Limotettix, individual clusters of species
that were associated merely on overall morphological
resemblance do not correspond well with the genetic
evidence from species that were barcoded.
Interpretation
Genetic affinities have been compared in seven separate iterations as more and more data have been added
to the leafhopper files, and repeatedly analyzed using
either sequences of >400 base pairs (the majority of
results) or using only full sequences (658 bp). Surprisingly, analysis of full sequences alone failed to give more
reliable results, deviating more from the morphological
analysis than when incorporating less complete data.
Having fewer species available for analysis, even under
more rigorous criteria, apparently upsets recovery of
natural affinities in neighbor-joining analysis.
Iterative analysis also showed that, as species were
added to neighbor-joining cladograms, the resulting divergences from the basal clades became more
American Entomologist • Volume 60, Number 1
Fig. 3. Interpreting barcode “trees.” A, data from neighbor-joining analysis as presented by Barcode of Life Database (BOLD)
system; B, phylogeny with minor variances (<1.5%) removed
and irregularities smoothed out by reattaching misplaced lineages using morphological criteria (inferred links indicated by
dashed lines). Iterations show that the largest discrepancies
are caused by the small number of species studied as these
usually disappear when more taxa are added to the tree.
regular in length. But in cases where major differences in divergence lengths were found in adjacent lineages, it was noted that morphological data seldom
supported these clades, suggesting homoplasy in the
genetic data. Realigning cladograms that have few
representative species using morphological criteria
usually eliminated major discrepancies in the lineages (Fig. 3). This suggests that, in recent clades where
few cases of extinction are probable, barcode phylogenies based on most of the known species of a genus
give evidence of constant rates of genetic change, a
so-called “genetic clock.”
If this is true, then we have an unique window through
which we can view evolution. One of the first things we
learn is the hugely different rates of change in allied
lineages. If you compare the genetic cladograms for
17
European members of Aphrodini and nearctic representatives of Xestocephalini (Fig. 3), you will see that
although there is a similar genetic divergence, this is
not reflected in morphological change. Aphrodini contains at least two genera that differ strikingly in head
structure, leg spination, and male genitalia, whereas
our Xestocephalini are so similar morphologically that
all the Nearctic species were incorrectly synonymized
in the most recent revision (Cwikla 1985).
Nor are cryptic species always genetically divergent;
Aphrodes contains two “sibling” species adventive to
different parts of North America (Hamilton 1975) that
have few or no genetic differences expressed in the
18
Fig. 4. Simplified phylogeny of 25 species groups representing
36 species of telamonine treehoppers (Membracidae) based on
barcode data. Photographs used with permission: A, Helonica
extrema by Sam Houston; B, Thelia bimaculata by Stephen
Cresswell; C, Carynota mera by Rob Curtis; D, Palonica viridis
by Claude Pilon; E, Carynota stupida by Steve Marshall; F, Glossonotus acuminatus by Carol Wolf; G, Heliria cristata by Paul
A. Scharf; H, Telamona concava by David E. Reed; J, Archasia
galeata by Mike Quinn; inset at top of page, morphological
outgroup (Telamonanthe pulchella), image from Oregon State
University collection. Scale line at bottom: 5% genetic change.
barcode sequence. Morphological change can be so
rapid in treehoppers (Hemiptera: Membracidae) that
it hardly registers in the regular cycle of mitochondrial
American Entomologist • Spring 2014
change. For example, the putative genera of Telamonini
are differentiated only by their obvious differences in
pronotal shape, but genetics supports morphological
studies (Wallace 2011, Hamilton 2011) that indicate these
changes are neither correlated nor indeed sequentially derived. Not only do members of the same genus
appear at widely spaced intervals within the phylogeny (Fig. 4), but very different-looking species presently
assigned to different genera (E, J in Fig. 4) appear to
be closely related, and three representatives of different putative genera (F-H in Fig. 4) differ by less than
1%. Clearly, treehopper genera that are based only on
pronotal shape need to be re-evaluated for monophyly.
Setting the Clock
Errhomus, whose species were divided by volcanism
and canyon formation, provides the geological evidence
needed to convert the relative genetic divergence data
into an absolute time scale. The largest data set in this
genus and the one most consistent across all taxa is the
0.5% difference between subspecies of Errhomus divided
from each other by the formation of Hell’s Canyon at 1.6
myBP (indicated in blue on Fig. 2). Several other such
subspecies farther downstream suggest that the greatly
enhanced flow of the lower Columbia River (when the
Snake River augmented its catchment basin) changed
other portions of its course to create additional subspecies of Errhomus. This suggests that 1% change in
the barcoding DNA occurs in approximately 3 million
years (allowing for the degree of variation commonly
found in each species, there is a standard variation of
about ±1.5 my). Using this criterion, additional parts of
the phylogeny of Errhomus can be correlated to known
changes in the course of the Columbia River (indicated
by purple and yellow on Fig. 2) and extinction events
(indicated in red) associated with volcanism in both
Washington and Idaho (Waitt and Swanson 1987, Leeman et al. 2008).
A truly remarkable amount of information can be
gleaned from such considerations. Of chief interest to
this particular study is the well-documented way in
which leafhoppers of the genus Flexamia have evolved
on successive genera of dominant and subdominant
grasses. This implies that, at geologically different eras,
particular grasses became dominants capable of sustaining long-term monophagy among their associated
leafhoppers. In Flexamia, the barcode changes delineating these species groups is sufficiently well defined
to permit determining the sequence in which nearctic
grasslands appear to have been dominated by various
grass genera. Combining overall topology of the Flexamia phylogeny with “genetic clock” values derived
from the phylogeny of Errhomus (1% divergence to 3
my) yields a complete timeline. Muhly grasses appear
to have dominated from the end of the Oligocene (25
myBP) until displaced in the lower Miocene (18 myBP)
by dominant grama grasses more suited to cooler climates, and afterwards with a modern admixture of
three-awn, bluestems, and buffalograss by mid-Miocene
(15 myBP). It is notable that all such suites of numerous
American Entomologist • Volume 60, Number 1
leafhopper species feeding on the same grass genera
are confined to “warm-season” grasses that germinate
during the heat of midsummer, as does crab grass.
By contrast, the leafhopper faunas of cool-season
grasses are mostly generalists assembled from many
grass-feeding genera. These species usually feed on a
variety of genera of grasses, indicating that leafhopper
genera were already in existence before cool-season
grasses became subdominant on the prairies. Only one
genus, Commellus Osborn & Ball, specializes on particular genera of cool-season grasses. Its basal member, C.
planus Thomas, is known only from Great Basin wild
rye (Elymus cinereus); its association with this spectacularly large host probably goes back well into the Oligocene, as it has diverged from related genera by 10%
(30 myBP). Other members of the genus are found on
smaller species of wild rye and on wheatgrasses (Agropyron), except for C. colon (Osborn & Ball), which is a
specialist on needle grass (Stipa). Specimens of Commellus successfully barcoded to date give minimum
ages for association with both Agropyron and Stipa
as 20 myBP (lower Miocene). Only three other cases
of sister-species of leafhoppers feeding on the same
cool-season grasses on the prairies are verified to date:
Hecalus major (Osborn) and H. montanus (Ball), the
platyrhynchus group of Attenuipyga (Hamilton 2000),
and the caprillus group of Mocuellus (Hamilton 1983),
all on wheatgrasses and all with a maximum divergence
of 1.7%. These considerations imply that cool-season
grasses arose at high elevations during the Oligocene,
only later dispersing to lower levels and becoming
subdominants on the prairies during the Pliocene,
about 5 myBP. This is consistent with a date just above
5.3 myBP (“across” the Pliocene boundary: Cerling et
al. 1997) for a shift from warm-season to cool-season
grasses in North American plains based on the teeth
of grazing mammals.
Using the ratio of 1% divergence to 3 my, it is possible to determine when nearctic species with closely
related Asian “sibling” species were separated by the
submerging of the Bering land bridge. For example, the
nearctic species of Cosmotettix Ribaut (=Palus DeLong
& Sleesman) have diverged by an equal degree (10%)
from the palaearctic C. costalis (Fallén), suggesting
that they separated in the Oligocene (30 myBP). Pairs
of other grassland leafhoppers (in Lebradea Remane,
Macustus Ribaut and Pinumius Ribaut, each with 4.7-5%
divergence) suggest that a more recent temperate-zone
land bridge allowed faunal exchange between the Old
World and the New in the mid-Miocene (14-15 myBP).
The latter date is confirmed by botanical evidence that
a common holarctic temperate forest was sundered and
replaced by separate palaearctic and nearctic boreal
forests in late Miocene times (Wolfe & Leopard 1967).
Boreal faunal exchanges in five genera that are predominantly Old World palaearctic in origin date to
only 5-6 my BP. These Pliocene dispersals resulted in
22 nearctic species that represent the descendants of
comparatively recent immigrants to North America:
one species of Paluda, three of Diplocolenus Ribaut,
19
four of Mocuellus Ribaut, six of Elymana DeLong, and
seven of Rosenus Oman. It is curious that these more
recent immigrants have both speciated more, and also
diverged more from the morphology of their palaearctic relatives than the earlier immigrants, an effect that
needs to be explored in greater detail.
From all these results, it is apparent that the species
examined in this study are of enormously different
ages. Some of them, like the two species of Pinumius,
seem to have diverged in the Miocene, while others
appear to be of much more recent origin. The highly
restricted grasslands of the Pacific Northwest are particularly rich in such closely related species (Hamilton
2002), with Hebecephalus DeLong having 16 of its 27
species restricted to these sites (Hamilton 1998). This
genus displays the greatest male genital differences wherever species exhibiting <2% genetic change
are in close contact (Fig. 5), suggesting that character
displacement by sexual selection during the Pliocene
was the driving evolutionary force at work. Another
example of character displacement, easier to identify
because it can be recognized without dissection, occurs
in the two species of the leafhopper genus Helochara
Fitch in the Pacific Northwest. These species feed on
Fig. 5. Phylogeny of 25 species of the grassland leafhopper
genus Hebecephalus with most closely related species in boxes:
red boxes for species occurring together that exhibit genital
character displacement, and a blue box for two allopatric species that show only trivial divergences.
20
“… it is apparent that the species
examined in this study are of
enormously different ages. Some
of them, like the two species of
Pinumius, seem to have diverged in
the Miocene, while others appear to
be of much more recent origin.”
different hosts: salt grass (Distichlis stricta) and toad
rush (Juncus bufonius). They both shift their overall
body size so that there is no overlap wherever they
coexist (Hamilton 1986). These species have only 0.20.4% barcode variation and 0% separation, indicating
a Quaternary origin; and the incomplete nature of the
character displacement shows that the morphological
changes are ongoing.
It is possible to make wider deductions using the same
ratio of 1% divergence to 3 my. For example, nearctic
insect genera apparently developed rapidly during the
Oligocene to early Miocene (see sidebar) when world
temperatures had declined from the pan-tropical conditions of the Eocene (Zachos et al. 2008) and a stable
holarctic fauna had developed. On the same basis, the
oldest leafhopper genera in North American grasslands
can be dated back to the Eocene, with characteristic
shrub-inhabitants of grasslands dating back at least 42
myBP. Their grass-feeding genera evolved later, but at
least as early as 36 myBP, soon after the Madro-tertiary
flora became differentiated on southwestern drylands
and grasslands first appeared (Axelrod 1958). North
American grasslands thus appear to predate the evolution of their characteristic mammalian fauna, but dominance of cool-season grasses in northern sites evolved
in synchrony with animals that could eat such grasses.
What of the deep past? The K/T breakup of Gondwanaland at 65 myBP should be represented in the BOLD
library by approximately 22% genetic change. Data
from faunas isolated in remote parts of the world by
this event are needed to fix this divergence/time scale
relationship, such as the Peloridiidae and Myerslopiidae of Chile and New Zealand (China 1962, Hamilton
1999), or the southern hemisphere spittlebugs of the
tribe Aphrophorini (Anyllis Kirkaldy in Austalia, Pseudaphronella Evans in New Zealand, Pseudaphrophora
Schmidt from Chile, and Napotrephes Stål from South
Africa). With more such data and refined genetic techniques, it may be possible to extend the range of our
investigations to the Cretaceous origins of the modern
flora. However, preliminary evidence suggests that, for
the few older lineages where changes are higher than
20% and biogeographic evidence links them to the
breakup of Gondwanaland, the divergence rate may
be as little as 1% = 4 my. Possibly this indicates that,
American Entomologist • Spring 2014
as changes accumulate over the millennia, evidence of
previous genetic divergence is more likely to be obliterated by new genetic changes. This apparent rate of
genetic change becomes still lower in older lineages.
Aleyrodoidea, one of the most ancient of Hemipteran
lineages, shows less than 30% genetic change from the
closest relatives (unpublished BOLD data), and still
more remote connections (e.g., to thrips) are impossible to retrieve.
Conclusions
Genetic “barcoding” is still in its infancy, but we can
already see that it may be the key to successfully unraveling complex biological patterns that predate modern ecosystems. Its ability to provide a standardized
time frame for Tertiary evolutionary events is unique.
This gives us an opportunity to mesh taxonomic data
with geological and paleoecological data to produce a
comprehensive analysis of the factors that produced
much of our present biota. It also serves as a scientific
check on taxonomic and evolutionary assumptions,
forcing us to admit our failures and shedding light on
the unexpected successes of some early taxonomists
(e.g., in defining accurately the genera Chlorotettix
Van Duzee, Ollarianus Ball, and Paraphlepsius Baker,
which have highly diverse male genitalia). It offers us
a chance to unite detailed local perspectives to identify global patterns. All these aspects of genetic data
are necessary for any understanding of how modern
ecosystems have evolved.
Taking the best evidence to date, barcoding gives an
approximate ratio of 1% genetic change = 3 (±1.5) million years for at least the latter half of the Tertiary, when
holarctic ecosystems were evolving. This is confirmed
at every point with known evidence of the origins and
dispersal of grasslands and their megafauna; but only
the immense fauna of leafhoppers can show us which
genera of grasses became abundant first, and where they
probably originated. It is now apparent that grasslands
and their rich fauna of endemic leafhoppers have coexisted since at least the Oligocene, with characteristic
shrub-inhabitants of grasslands dating back at least
to the Eocene and many leafhopper genera evolving
to feed on grasses in synchrony with the evolution of
the Madro-tertiary flora. These grassland genera also
track subsequent evolution of grassland flora down to
the Pliocene origin of cool-season grasses.
While barcoding appears to be useful across the
Tertiary, for more detailed analyses of events within
the Quaternary a more quickly evolving sequence is
needed. Perhaps we can find it elsewhere on the COI
gene that has much faster-evolving sections, or possibly by using the entire COI gene that records events
across only about 1.2 my for each 1% genetic change
(Caccone and Sbordoni 2001).
Perhaps now we have the full suite of tools needed
to find out how insect species evolve, and just how this
occasionally happens in a geologically short space of
time. This hypothesis requires further testing. Examination of speciation events in other environments
American Entomologist • Volume 60, Number 1
How old are genera?
Nearctic leafhoppers belonging to genera without neotropical species
can be estimated to have first appeared in specific geological ages by
genetic change recorded from each separate lineage (1% change =
3 million years). The first grass-feeding genera (boldfaced) appeared in
the late Eocene, and the rate at which subsequent new genera were
created rises rapidly with climate change during the Oligocene, tapering
off as temperate-zone ecosystems become established in the Miocene.
An asterisk (*) indicates a genus with few barcoded old-world palaearctic
species, in which case the age of its lineage is probably underestimated.
Eocene:
c. 45 myBP
Tiaja, Tinobregmus
c. 42 myBP
Errhomus, Lystridea
c. 39 myBP
Acinopterus, Ceratagallia, Davidsonia, Eupteryx, Koebelia,
Ossiannilssonola
c. 36 myBP
Alebra, Amplicephalus, Arboridia, Balclutha, Cazenus,
Oncopsis, Pagaronia, Thatuna
Oligocene:
c. 33 myBP
Auridius, Carsonus, Crassana, Doliotettix, Eusama,
Gillettiella, Hardya, Hylaius, Limotettix, Ollarianus,
*Sonronius, Stenometopiellus, Twiningia
c. 30 myBP
Amblysellus, Athysanella, Ballana, Caladonus,
Calanana, Commellus, Conosanus, Coulinus,
Deltocephalus, Dikraneura, Doleranus, Drionia,
Gloridonus, Endria, Euscelis / Streptanus, Evacanthus,
Extrusanus, Flexamia, Graminella, Hebecephalus,
Idiocerus, Latalus, Lonatura, Macrosteles, Mesamia,
Osbornellus, *Paluda, Ribautiana, *Rosenus, Sanctanus,
Scaphoideus, Scaphytopius, Telusus, Texananus
c. 27 myBP
Aflexia, Aligia, Ankosus, Attenuipyga, Balcanocerus,
Bandara, Cabrulus, Cicadula, Cribrus, Daltonia,
Destria, Dixianus, Eutettix, Giprus, Gyponana, Hecalus,
Hecullus, Idiodonus, Laevicephalus, Lebradea,
Norvellina, Omanana, Orocastus, Paraphlepsius,
Phlepsanus, Pinumius, Reventazonia, Spathanus
c. 24 myBP
Alapus, Athysanus, Boreotettix, Colladonus, Crumbana,
Decua, Dorydiella, Edwardsiana, Empoa, Erythroneura,
Forcipata, Kansendria, Knullana, Limbanus,
Neohecalus, Nurenus, Peconus, Pendarus, Platymetopius,
Prairiana, Sorhoanus, Typhlocyba
Miocene:
c. 21 myBP
Cetexa, Cosmotettix, Dicyphonia, Driotura, *Elymana,
Eusama, Homalodisca, Lycioides, *Mocuellus, Neokolla,
Prescottia
c. 18 myBP
Bonneyana, Cantura, Cuerna, *Diplocolenus, Dragonana,
Marganana, Helochara, Hymetta, Psammotettix,
Rugosana
such as the Hawaiian islands might be able to verify
the molecular clock rate utilizing other Hemiptera,
and to compare it to rates of molecular evolution in
other orders.
Acknowledgments
Barcode sequence analyses were enabled by funding
from the Government of Canada through Genome Canada and the Ontario Genomics Institute in support of
the International Barcode of Life project. We thank Paul
21
Hebert and colleagues at the Canadian Centre for DNA
Barcoding of the University of Guelph for carrying out
the sequence analysis. Photographs were used with the
permission of Stephen Cresswell of Buckhannon, West
Virginia; Rob Curtis of Chicago, Illinois; Sam Houston
of Sand Springs, Oklahoma; Steve Marshall of Guelph,
Ontario; Tom Murray of Groton, Massachusetts; Claude
Pilon of Repentigne, Quebec; Paul A. Scharf of Lake
Gaston, NC; David E. Reed of Chanhassen, Minnesota;
Mike Quinn of Austin, Texas; Carol Wolf of Woodbury,
Tennessee, and Joanne Elsaesser of AAFC. The manuscript was read by C. Dietrich of the Illinois Natural
History Survey, Champaign.
References Cited
Axelrod, D.I. 1958. Evolution of the Madro-tertiary geoflora. Bot. Rev. 24(7): 433-509.
Barcode of Life Datasystem (BOLD). http://www.
boldsystems as a public dataset (dx.doi.org/10.5883/
DS-EMAUCH0).
Caccone, A., and V. Sbordoni. 2001. Molecular biogeography, evolutionary rates, and morphological adaptation
to cave life: a case study using Bathysciinae beetles and
sequence data from the mitochondrial COI gene. Evolution 55: 122-130.
Cerling, T.E., J.M. Harris, B. J. MacFadden, M.G. Leakey, J.
Quade, V. Eisenmann, and J.R. Ehleringer. 1997. Global
vegetation change through the Miocene/Pliocene boundary. Nature 389: 153-158.
China, W.E. 1962. South American Peloridiidae (Hemiptera-Homoptera: Coleorrhyncha). Trans. R. Entomol.
Soc. London 114: 131-161.
Cwikla, P.S. 1985. Classification of the genus Xestocephalus (Homoptera: Cicadellidae) for North and Central
America including the West Indies. Brenesia 24: 175-272.
Dietrich, C.H., R.F. Whitcomb, and W.C. Black, IV. 1997.
Phylogeny of the grassland leafhopper genus Flexamia
(Homoptera: Cicadellidae) based on mitochondrial DNA
sequences. Molec. Phylog. Evol. 8(2): 139-149.
Gillespie, R.G. 2005. The ecology and evolution of Hawaiian spider communities. Amer. Scientist 93: 122-131.
Hamilton, K.G.A. 1975. A review of the northern hemisphere Aphrodina (Rhynchota: Homopterea: Cicadellidae), with special reference to the nearctic fauna. Canad.
Entomol. 107: 1009-1027.
Hamilton, K.G.A. 1983. Introduced and native leafhoppers common to the old and new worlds (Rhynchota:
Homoptera: Cicadellidae). Canad. Entomol. 115: 473-511.
Hamilton, K.G.A. 1986. Revision of Helochara Fitch (Rhynchota: Homoptera: Cicadellidae). J. Kans. Entomol. Soc.
59: 173-180.
Hamilton, K.G.A. 1994. Evolution of Limotettix Sahlberg
(Homoptera: Cicadellidae) in peatlands with descriptions
of new taxa. Mem. Entomol. Soc. Canada 169: 111-133.
Hamilton, K.G.A. 1998. New species of Hebecephalus DeLong from British Columbia, Idaho and adjacent states
(Rhynchota: Homoptera: Cicadellidae). J. Entomol. Soc.
Brit. Columb. 95: 65-80.
Hamilton, K.G.A. 1999. The ground-dwelling leafhoppers
Myerslopiidae, new family and Sagmatiini, new tribe (Homoptera: Membracoidea). Invert. Taxon. 13(2): 207-235.
Hamilton, K.G.A. 2000. Five genera of new world “shovel-headed” and “spoon-bill” leafhoppers (Hemiptera:
Cicadellidae: Dorycephalini and Hecalini). Canad. Entomol. 132: 429-503.
22
Hamilton, K.G.A. 2002. Homoptera (Insecta) in Pacific
Northwest grasslands. Part 2 - Pleistocene refugia and
postglacial dispersal of Cicadellidae, Delphacidae and
Caliscelidae. J. Entomol. Soc. Brit. Columb. 99: 33-80.
Hamilton, K.G.A. 2006. Beyond ecology: bugs reveal the
deep roots of modern ecoregions, pp. 95-100. In D. Egan
and J.A. Harrington, Eds. The conservation legacy lives
on... Proceedings of the 19th North American Prairie
Conference (University of Wisconsin-Madison, WI).
Hamilton, K.G.A. 2011. What we have learned from shutterbugs. Amer. Entomologist 57 (2): 102-109.
Hamilton, K.G.A. and R.S. Zack. 1999. Systematics and
range fragmentation of the Nearctic genus Errhomus
Oman (Rhynchota: Homoptera: Cicadellidae). Ann. Entomol. Soc. Amer. 92(3): 312-354.
Leeman, W.P., C. Annen, and J. Dufek. 2008. Snake River Plain – Yellowstone silicic volcanism: implications
for magma genesis and magma fluxes, pp. 235-259. In:
C. Annen and G.F. Zellmer (eds.), Dynamics of Crustal
Magma Transfer, Storage and Differentiation. Geological
Society, London, Special Publications 304.
McKamey, S. 2001. Revision of the nearctic species of Limotettix (Scleroracus Van Duzee) leafhoppers (Hemiptera:
Cicadellidae: Deltocephalinae). Proc. Entomol. Soc.
Wash. 103(3): 686-753.
Oman, P.W. 1987. The leafhopper genus Errhomus (Homoptera: Cicadellidae: Cicadellinae), systematics and
biogeography. Ore. State Univ. Syst. Entomol. Lab. Occ.
Publ. 1: 72 pp.
Oman, P.W. and C.A. Musgrave. 1975. The nearctic genera of Errhomenini (Homoptera: Cicadellidae). Melanderia 21: 1-14.
Rubinoff, D. unpublished. Patterns of ancient colonization of Hawaii’s most diverse moths (Hyposmocoma:
Cosmopterigidae). Oral presentation at Entomology
2013, Austin, Texas.
Waitt, R.B., Jr., and D.A. Swanson. 1987. Geomorphic evolution of the Columbia plain and river. In W.L. Graf [ed.],
Geomorphic systems of North America, chapter ii, Columbia and Snake River Plains. Geol. Soc. Am. (Centennial Spec. Vol.) 3: 403-468.
Wallace, M.S. 2011. Morphology-based phylogenetic analysis of the treehopper tribe Smiliini (Hemiptera: Membracidae: Smiliinae), with reinstatement of the tribe
Telamonini. Zootaxa 3047: 1-42.
Whitcomb, R.F., and A.L. Hicks. 1988. Genus Flexamia:
new species, phylogeny, and ecology. Gr. Basin Nat.
Mem. 12: 224-323.
Wilkins, S. 2013. The evolution of Cichlids. http://www.
cichlid-forum.com/articles/evol_cich_pt1.php. (accessed
10/29/2013).
Wolfe, J.A., and E.B. Leopard. 1967. Neogene and Early
Quaternary vegetation of northwestern North America and northeastern Asia; Chapter 10: 193-206. In D.M.
Hopkins, ed., The Bering Land Bridge. Stanford University Press, Stanford, CA.
Zachos C., G.R. Dickens, and R.E. Zeebe. 2008. An early
Cenozoid perspective on greenhouse warming and carbon-cycle dynamics. Nature 451: 279-283.
Andrew Hamilton is a research entomologist at the Canadian National Collection of Insects, Arachnids, and Nematodes maintained by AAFC at the Central Experimental
Farm in Ottawa, ON. He has published extensively on the
biodiversity, evolution, paleontology, and classification
of Auchenorrhyncha and can be reached at hamiltona@
agr.gc.ca.
American Entomologist • Spring 2014