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Classification and Biogeography of Neotropical True Bugs

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Abstract

Abstract A review of Heteroptera classification, biogeography, and phylogeography is presented. The use of molecular data significantly expanded the knowledge of phylogenetic relationships among and within heteropteran infraorders. However, taxa historically less studied continue to receive little attention. Promising, new molecular approaches with increased genetic markers and broader taxon sampling, as well as new morphological approaches (e.g., microtomography), are the future for more stable classifications and a better comprehension of the heteropteran evolutionary history, but their application is still incipient. A non-exhaustive overview of studies about Neotropical heteropteran biogeography is made and discussed, including those about intercontinental connections and regional distribution patterns. The most comprehensible studies, and more promising area, seem to be the one focused on distribution patterns, especially employing macroecological methods, and trying to elucidate what are the major factors responsible for the distribution of the group in the Neotropics. Finally, we present an overview of phylogeographic studies involving Neotropical Heteroptera. It is clear that the best biogeographic and phyllogeographic studied groups are those with medical and economical importance (e.g., Reduviidae and Pentatomidae).
57© Springer Science+Business Media Dordrecht 2015
A.R. Panizzi, J. Grazia (eds.), True Bugs (Heteroptera) of the Neotropics,
Entomology in Focus 2, DOI 10.1007/978-94-017-9861-7_3
Chapter 3
Classifi cation and Biogeography
of Neotropical True Bugs
Augusto Ferrari , Kim R. Barão , Filipe M. Bianchi ,
Luiz A. Campos , and Jocélia Grazia
Abstract A review of Heteroptera classifi cation, biogeography, and phylogeography
is presented. The use of molecular data signifi cantly expanded the knowledge of
phylogenetic relationships among and within heteropteran infraorders. However,
taxa historically less studied continue to receive little attention. Promising, new
molecular approaches with increased genetic markers and broader taxon sampling,
as well as new morphological approaches (e.g., microtomography), are the future
for more stable classifi cations and a better comprehension of the heteropteran evo-
lutionary history, but their application is still incipient. A non-exhaustive overview
of studies about Neotropical heteropteran biogeography is made and discussed,
including those about intercontinental connections and regional distribution patterns.
The most comprehensible studies, and more promising area, seem to be those
focused on distribution patterns, especially employing macroecological methods,
and trying to elucidate what are the major factors responsible for the distribution of
the group in the Neotropics. Finally, we present an overview of phylogeographic
studies involving Neotropical Heteroptera. It is clear that the best biogeographic
and phylogeographic studied groups are those with medical and economical impor-
tance (e.g., Reduviidae and Pentatomidae).
A. Ferrari (*)
Instituto de Ciências Biológicas (ICB) , Universidade Federal do Rio Grande - FURG ,
Campus Carreiros - Av. Itália, km 8, Prédio 6, Sala 22g , Rio Grande , RS 96203-900 , Brazil
e-mail: ferrariaugusto@gmail.com
K. R. Barão F. M. Bianchi
Programa de Pós-Graduação em Biologia Animal, Instituto de Biociências , Universidade
Federal do Rio Grande do Sul (UFRGS) , Av. Bento Gonçalves 9500, prédio 43435, Bairro
Agronomia , Porto Alegre , RS 91501-970 , Brazil
e-mail: kbarao@gmail.com; fmichels2@gmail.com
L. A. Campos J. Grazia
Departamento de Zoologia, Instituto de Biociências , Universidade Federal do
Rio Grande do Sul (UFRGS) , Av. Bento Gonçalves 9500, prédio 43435, Bairro Agronomia ,
Porto Alegre , RS 91501-970 , Brazil
e-mail: luiz.campos@ufrgs.br; jocelia@ufrgs.br
58
3.1 Introduction
The knowledge of the Heteroptera goes back to the eighteenth century, during the
1750s to 1770s. This period was called “Classical” (Slater 1974 ) and began with
C. Linnaeus, followed by J.C. Fabricius and others, which studied the Heteroptera
in general and provided the fi rst major higher classifi cations of the suborder.
Carl Stål, from the mid-1850s to the end of the 1870s, represents the watershed of
the revisional studies in many heteropteran families (Stål 18701876 ). The
appearance of specialized works started in 1870, primarily in Europe, favored by the
enrichment of the European museums by major collecting expeditions in all parts of
the world. It was a period of dominance for taxonomy, not only with descriptive
works but also with faunistic (e.g., Distant 18801893 ) and comprehensive catalogs
(e.g., Lethierry and Severin 18931896 , a general catalog, and Kirkaldy 1909 ,
a Rhynchota catalog). From the seventeenth to the early twentieth centuries, not so
many heteropterists were dedicated to describe new taxa in the New World, and
mostly faunistic works were done (Mayr 1864 , 1866a , b ; Uhler 1869 , 1894 ;
Berg 1879 , 1884 – Hemiptera Argentina; Bergroth 1891 , 1893 , 1894 , 1905 , 1908 ,
1914 , 1918 ; Breddin 1903a , b , c , d , 1904a , b , c , d , 1907 , 1908a , b , 1909 , 1910 ,
1912a , b , c , 1914 ).
Reuter ( 1910 ) pioneered in evaluating the classifi cation of Heteroptera, making
explicit interpretations of the characters used by previous authors, presenting objec-
tive arguments for defi nition of groups (Schuh 1986 ), and producing a phylogenetic
scheme for the Hemiptera. As in many other works, character polarity was the
weakest aspect in Reuter’s work (Schuh and Slater 1995 ). Although Reuter ( 1910 )
proposed subordinal names, most were never consistently adopted, but he already
had a close concept of the current Gerromorpha, Nepomorpha, and Cimicomorpha.
For a more complete view of Reuter’s work, see Schuh and Slater ( 1995 ).
From 1900 to the early 1940s, several workers have devoted to the description of
new genera and species. For their infl uence in the knowledge about classifi cation of
Neotropical Heteroptera, worth to mention is the world catalog of part of the fami-
lies’ currently classifi ed in Pentatomoidea (Kirkaldy 1909 ) and the world revision
of Thyreocoridae (McAtee and Malloch 1933 ). Other relevant taxonomists in this
period were G. Breddin, E.E. Bergroth, R. Jeannel, H.G. Barber, G. Horvath, and
E.P. Van Duzee.
From the early 1950s to the beginning of the 1990s, taxonomists focused mainly
on the revision and description of taxa within families. Outstanding exceptions are
the world catalogs for genera and species of Miridae (Carvalho
1952 ; Schuh 1995 ,
20022013 ), Tingidae (Drake and Ruhoff 1960 , 1965 ; Froeschner 1996 , 2001 ),
Lygaeidae (Slater 1964 ; Slater and O’Donnell 1995 ), and the world classifi cation
reviews of Aradidae (Usinger and Matsuda 1959 ) and Cimicidae (Usinger 1966 ).
Other relevant taxonomists in this period were T. Esaki and H.B. Hungerford
for Nepomorpha and Gerromorpha, respectively; D. Leston for Cimicoidea;
R. Cobben for Leptopodomorpha; R. Matsuda for Gerridae; P.W. Wygodzinsky
for Enicocephalomorpha, Dipsocoromorpha, and Reduviidae; P.D. Ashlock for
A. Ferrari et al.
59
Lygaeidae; and R. Ruckes, L.H. Rolston, M. Becker, and A.A. Pirán for
Pentatomidae. For an extensive review of the world major taxonomists in
Heteroptera, see Schuh and Slater ( 1995 ).
In a wider classifi cation approach within the Heteroptera, the work of Leston et al.
( 1954 ) was a keystone to heteropteran modern classifi cation. Leston et al. introduced
the terms Cimicomorpha and Pentatomomorpha in the fi rst attempt to recognize nat-
ural groups within the polyphyletic Geocorisae, based on accumulated evidence from
comparative studies of internal anatomy and external morphology of the Heteroptera
(Schuh and Slater 1995 ). The infl uence of Leston et al. work was widely felt and
stimulated other authors into attempting to document the monophyly of higher
groups within Heteroptera. As outlined by Štys and Kerzhner ( 1975 ), such attempts
resulted in the recognition of seven infraorders, which at the time were not proposed
based on cladistic analysis: Enicocephalomorpha Stichel; Dipsocoromorpha
Miyamoto; Gerromorpha Popov; Nepomorpha Popov; Leptopodomorpha Popov;
Cimicomorpha Leston, Pendergrast, and Southwood; and Pentatomomorpha Leston,
Pendergrast, and Southwood.
3.2 Phylogenetic Systematics and Modern Higher
Classifi cations of Heteroptera
Hennig’s ideas on defi ning and recognizing monophyletic groups based on shared
derived characters (i.e., synapomorphies) took some time to infl uence the classifi cation
of Heteroptera, even after the publication of its English edition (Hennig 1950 , 1966 ).
The fi rst studies to apply the concepts proposed by Hennig were approximations of
what is now traditionally called “cladistic analysis” – based on characteristics usually
employed in taxonomy and comparative morphology, such works aimed to identify
equivalence between phylogenetic hypotheses and taxonomic classifi cations (Schuh
1979 , 1986 ). At higher taxonomic ranks, such hypotheses of relationships were pre-
sented as hierarchical branching diagrams, depicting the distributional congruence of
attributes (characters) between taxa. At the time of Hennig’s work, important aspects of
phylogenetic analysis, such as broad sampling of outgroups and questions about root-
ing, character polarity, and character coding had not yet been developed. Nevertheless,
Hennig’s legacy laid the foundations to produce a general reference system for biology
based exclusively on monophyletic groups and a way to summarize the knowledge
contained in classifi cations and taxa diagnoses (Schuh 1986 ).
The 1970s and 1980s saw the rapid development of phylogenetic methods and an
arising dispute between schools of thought (evolutionary systematics, numerical
taxonomy or numerical phenetics, and systematic cladistics) for the establishment
of the most suitable classifi cation method (Hull 1988 ). It was not clear which were
the most appropriate methods for assessing phylogenetic relationships neither if this
would be a task that could be achieved in the near future.
On his seminal work on adult and immature heteropteran morphology, Cobben
(
1968 , 1978 ) provided cues for the defi nition of characters within Heteroptera and
3 Classifi cation and Biogeography of Neotropical True Bugs
60
enormously expanded the knowledge about features never studied before. Cobben’s
sampling of the Neotropical fauna was notable, by sampling species from the
Antilles, Costa Rica, Brazil, and Chile in its fi rst volume (Cobben 1968 ), then, on
its second volume, by extending the Neotropical sampling to species occurring in
Honduras, Paraguay, Peru, and Trinidad (Cobben 1978 ). Cobben’s studies on heter-
opteran morphology would be later compiled in morphological matrices (Schuh
1979 ; Mahner 1993 ; Wheeler et al. 1993 ), but many characters proposed by Cobben
are yet to be coded in a formal cladistic analysis (Weirauch and Schuh 2011 ).
Cobben ( 1978 ) also ventured into proposing phylogenetic relationships within
Heteroptera, even though not using formal cladistic analysis. Cobben recognized
Gerromorpha as paraphyletic and at the base of Heteroptera. Schuh ( 1979 ) reaccessed
Cobben’s work employing cladistic analyses, proposing the fi rst phylogenetic analysis
using parsimony criterion and outgroup comparison to polarize characters, in order to
recognize higher-level groups in Heteroptera. Schuh ( 1979 ) demystifi es wrong concepts
implicit in Cobben’s work, such as the impossibility to cladistically analyze higher taxa
of Heteroptera because of the enormous amounts of parallelisms. Schuh ( 1979 ) found
the Enicocephalomorpha to be the sister group to the remaining Heteroptera,
Dipsocoromorpha as sister group to Neoheteroptera, and Gerromorpha as sister group
to Nepomorpha + Leptopodomorpha and Cimicomorpha + Pentatomomorpha.
Since Schuh’s reanalysis of Cobben’s work, phylogenetic analyses based on
morphological and molecular datasets have increasingly infl uenced the understand-
ing of relationships within Heteroptera, resulting in explicit cladistic hypotheses of
relationships among the seven infraorders (Weirauch and Schuh 2011 ). Wheeler
et al. ( 1993 ) hypothesis treats the Enicocephalomorpha as the sister group to the
remaining Heteroptera, Dipsocoromorpha as sister group to the Neoheteroptera,
Gerromorpha as sister group to the Panheteroptera, and Nepomorpha as sister taxon
to the Leptopodomorpha (Cimicomorpha + Pentatomomorpha).
Other competing hypotheses, based on morphological data of fossil and extant
taxa, include Nepomorpha as the sister taxon to the remaining Heteroptera (Mahner
1993 ; Scherbakov and Popov 2002 ), without resolving the relationships among the
other infraorders. Li et al. ( 2012 ), based on molecular data, agree with the
Nepomorpha as sister taxon to the remaining Heteroptera, but fi nd the
Dipsocoromorpha + Gerromorpha as sister taxon to Enicocephalomorpha + Leptopo-
domorpha and Cimicomorpha + Pentatomomorpha. Yet, others agree with Wheeler
et al. ( 1993 ) with the Enicocephalomorpha as the sister taxon to the remaining
Heteroptera, but disagree on the relationships of other infraorders (Xie et al. 2008 ).
The only sister-group relationship that is not contradicted by any of these hypoth-
eses is the Cimicomorpha + Pentatomomorpha. This clade was also supported in
combined morphological and molecular analysis by Schuh et al. ( 2009 ) and in mor-
phological analysis focusing on the rhabdom structure of the ommatidia (Fischer
et al. 2000 ).
Spangenberg et al. ( 2013 ) provided new data on head morphology (including
musculature, tentorium, cephalic nervous system, and alimentary tract) based on
serial sectioning and computer-based 3D reconstruction for representatives of the
potentially basal heteropteran lineages (Enicocephalomorpha, Dipsocoromorpha,
A. Ferrari et al.
61
and Gerromorpha). Spangenberg et al. cladistically analyzed 71 cephalic characters
scored for 16 heteropteran terminals. Heteropteran monophyly was strongly sup-
ported, but some of the recovered relationships between infraorders are not consistent
with previous studies, such as the paraphyly of Nepomorpha and Dipsocoromorpha –
the authors thus suggest that cephalic features alone are apparently insuffi cient for a
clarifi cation of the relationships of the major lineages of Heteroptera. They also
mapped cephalic character data on three alternative hypotheses, being Wheeler et al.
( 1993 ) the most parsimonious one, requiring 201 steps for their data. The topologies
of Xie et al. ( 2008 ) and Mahner ( 1993 ) required 202 and 212 steps, respectively.
There has been a recent increase in studies employing DNA data, especially those
with a more comprehensive taxon sampling. The availability of new sequencing
techniques promises a revolution, by reducing costs and increasing the availability
of molecular data. Phylogenomics and proteomics approaches are making possible
a better understanding of the relationships within Insecta (e.g., http://www.1kite.
org/index.html ). At the same time, the availability of molecular data is increasing, as
is the refi nement of morphology-driven studies with the diffusion of new approaches.
New and improved technology for image capture and treatment, such as confocal
microscopes and 3D-reconstructions by scanning electron microscopy and X-ray
microtomography, are making possible to revisit and investigate underexplored mor-
phological characters (Friedrich et al. 2014 ). The new challenge will be to integrate
new molecular and morphological datasets enabling its combined analysis, as has
been recently done by some researchers (Friedrich et al. 2014 ).
3.2.1 Phylogenetic Relationships Within
the Heteropteran Infraorders
Nothing is known about the phylogenetic relationships within Enicocephalomorpha.
Therefore, phylogenetic relationships will be presented for the remaining six
infraorders of Heteroptera.
Dipsocoromorpha
According to Weirauch and Štys ( 2014 ), the Dipsocoromorpha are the least docu-
mented heteropteran infraorder, comprising about 300 species in fi ve families. The
monophyly of the group has been considered to be controversial because its families
show a great morphological variability (Weirauch and Schuh 2011 ). Weirauch and
Štys ( 2014 ) were the fi rst authors to comprehensively sample the Dipsocoromorpha
and perform a phylogenetic analysis of this infraorder. Their results support a mono-
phyletic Dipsocoromorpha, as well as the families included in the analysis (i.e.,
Ceratocombidae, Dipsocoridae, and Schizopteridae). However, the position of this
infraorder in Heteroptera still needs to be settled, since the dataset alone (ribosomal
data) is not suffi cient to resolve deep relationships among the Heteroptera.
3 Classifi cation and Biogeography of Neotropical True Bugs
62
Gerromorpha
The infraorder Gerromorpha, commonly called the semiaquatic bugs, comprises
about 2,100 species in eight families (Damgaard 2008 ). Although the monophyly of
this taxon has been extensively corroborated (Andersen 1982 ; Damgaard 2008 ), the
monophyly and relationship among its superfamilies have been recently disputed
(Damgaard 2012 ). The pioneerism of Andersen’s contributions (Andersen 1981 ,
1982 ) is still the most comprehensive comparative study of this infraorder (Damgaard
2012 ). Damgaard ( 2008 ) proposed a phylogenetic hypothesis for Gerromorpha using
morphological and molecular data summarized from several studies (Muraji and
Tachikawa 2000 ; Andersen and Weir 2004 ; Damgaard et al. 2005 ; Damgaard and
Cognato 2003 ) addressing the systematics of major lineages within Gerromorpha.
Damgaard ( 2008 ) corroborated the monophyly of the infraorder, as well as the rela-
tionship of the Mesoveliidae as the sister group to all other gerromorphan families,
and the relationship between Gerridae and Veliidae. Gerroidea, Hydrometroidea,
Vellinae, and Cylindrostethinae were recovered as paraphyletic.
Nepomorpha
The Nepomorpha, or true water bugs, comprises about 2,000 species placed on 11
families. The monophyly of Nepomorpha is widely accepted (Wheeler et al. 1993 ;
Mahner 1993 ; Scherbakov and Popov 2002 ; Xie et al. 2008 ), but Hua et al. ( 2009 )
found contrasting results, suggesting Nepomorpha was paraphyletic and the Pleidae
should be elevated to infraordinal level, i.e., Pleomorpha; given their small taxon
sample and lack of a combined effort including morphology, their taxonomic deci-
sions have not been accepted (Weirauch and Schuh 2011 ).
Within Nepomorpha, there is an agreement in placing the Nepidae +
Belostomatidae as the sister group to the remaining Nepomorpha and in treating
the Helotrephidae, Notonectidae, and Pleidae as a clade (Rieger 1976 ; Mahner
1993 ; Hebsgaard et al. 2004 ).
Leptopodomorpha
About 400 species distributed in four families comprise the Leptopodomorpha, or
shore bugs. Family-level relationships within the infraorder have not changed since the
publication of Schuh and Polhemus ( 1980 ) that, based on morphological data, pro-
posed Saldidae + Aepophilidae to represent the sister group to Omaniidae +
Leptopodidae. Recently, Zhang et al. ( 2014 ) found the same relationships among the
extant leptopodomorphan families, placing the fossil Palaeoleptidae as sister group to
Omaniidae + Leptopodidae, and the fossil Archegocimicidae more closely related to
Aepophilidae. Other phylogenetic contributions to the Leptopodomorpha are the cla-
distic revisions of Saldula Van Duzee and of Pseudosaldula Cobben (Lindskog and
Polhemus
1992 ; Schuh and Polhemus 2009 ).
A. Ferrari et al.
63
Cimicomorpha
Cimicomorpha is the largest infraorder of Heteroptera, comprising about 20,000
species in 16 families (Schuh and Slater 1995 ). The Cimicomorpha is a well-studied
infraorder, especially because of its economic and health importance; however, few
studies were concerned with the phylogenetic relationships within the family level
(Schuh et al. 2009 ). Ford ( 1979 ) and Kerzhner ( 1981 ) were the fi rst to propose
hypotheses of phylogenetic relationships within Cimicomorpha, but the phyloge-
netic relationships proposed by Schuh and Štys ( 1991 ) were the most accepted.
Since this publication, knowledge about cimicomorphan morphology has increased
for many families. Schuh and Slater ( 1995 ) made important new observations about
the Cimicomorpha morphology; other important contributors to the morphology of
the infraorder are Weirauch ( 2003 , 2005 , 2006 ), Schuh ( 2006 ), Popov ( 2008 ), and
Cassis et al. ( 1999 ).
Tian et al. ( 2008 ) analyzed the phylogenetic relationships of 12 cimicomorphan
families based on molecular dataset and different methods of phylogenetic recon-
struction, fi nding small differences from Schuh and Štys ( 1991 ), but did not propose
taxonomic changes. Analyzing molecular and morphological data, Schuh et al.
( 2009 ) found a paraphyletic Cimicomorpha, with the Thaumastocoridae as sister
group to the Pentatomomorpha, but the authors avoided taking taxonomic decisions
at the infraordinal level because of ambiguities between the datasets results. Within
the Cimicomorpha, Schuh et al. ( 2009 ) expanded the Cimiciformes to include the
Joppeicidae, Microphysidae, Velocipedidae, and Curaliidae; the monophyly of
Miroidea, Cimicoidea, Reduviidae, Tingidae, and Miridae were corroborated. At
family level or lower levels, families such as the Miridae (Weirauch and Schuh
2010 ), Reduviidae (Paula et al. 2005 , 2007 ; Weirauch 2008 ; Weirauch and Munro
2009 ; Hwang and Weirauch 2012 ), and Tingidae (Montemayor and Costa 2009 ;
Guilbert 2012a , b ; Guilbert et al. 2014 ) were analyzed phylogenetically, and the
Reduviidae has been the focus of studies on comparative morphological and behav-
ioral evolution (Berniker and Weirauch 2012 ; Weirauch et al. 2011 ; Zhang and
Weirauch 2013 ).
Pentatomomorpha
Infl uenced by the work of Tullgren ( 1918 ) and Singh-Pruthi ( 1925 ) and by their
own observations, Leston et al. ( 1954 ) coined the Pentatomomorpha to include the
Aradoidea and Trichophora. As conceived by Tullgren ( 1918 ), the Trichophora
gathered the taxa presenting ventral abdominal trichobothria and a certain type of
pulvilli ( sic arolia). As conceived by Leston et al. ( 1954 ), the Pentatomomorpha
could be recognized by wing venation, pretarsal structure, salivary glands, internal
genitalia, and egg morphology; the family composition of Pentatomomorpha little
changed after their work, with the exception of the Thaumastocoridae and Saldidae,
and Leptopodidae being transferred to Cimicomorpha and Leptopodomorpha,
respectively (Štys and Kerzner
1975 ).
3 Classifi cation and Biogeography of Neotropical True Bugs
64
Four to six superfamilies have been recognized within the Pentatomomorpha
(Štys 1961 ; Schaefer 1993 ; Carver et al. 1991 ; Schuh 1986 ; Henry and Froeschner
1988 ), illustrating the uncertainty of relationships in the infraorder. Currently, fi ve
superfamilies are accepted: Aradoidea, Coreoidea, Lygaeoidea, Pentatomoidea, and
Pyrrhocoroidea. So far, seven works have addressed the phylogeny of the
Pentatomomorpha, all fi nding the infraorder to be monophyletic and only the
Aradoidea and Pentatomoidea are consistently recognized as monophyletic (Henry
1997 ; Li et al. 2005 , 2006 ; Xie et al. 2005 ; Grazia et al. 2008 ; Hua et al. 2008 ; Tian
et al. 2011 ; Yao et al. 2012 ). The Aradoidea seems to be the sister group of
Trichophora, and the relationships within Trichophora are far from being under-
stood. Some phylogenetic hypotheses agree in Coreoidea and Lygaeoidea probably
being polyphyletic (Li et al. 2005 , 2006 ; Xie et al. 2005 ) and the Pyrrhocoroidea
sometimes appearing as sister group to Coreoidea + Lygaeoidea (Henry 1997 ; Xie
et al. 2005 ; Hua et al. 2009 ) or as sister group to the Pentatomoidea (Li et al. 2005 ,
2006 ) or to the Coreoidea (Tian et al. 2011 ).
3.3 Biogeography of Neotropical Heteroptera
Since the contributions of Augustin P. de Candolle and Friedrich W. H. A. von
Humboldt in the early nineteenth century, the Neotropical region has been the focus
of studies on how the geophysical processes infl uence the distribution of living
organisms (Llorente et al. 2000 ). From the very beginning, naturalists studying the
Neotropical biota were amazed by its richness and diversity and were puzzled on
how to explain the biogeographical evolution of such a diverse ecosystem. Most of
the questions made by the fi rst naturalists remain unanswered: Are there distribu-
tional patterns? And how can they be explained? Are distributional patterns similar
to all organisms or each taxon responds differently to it? How is the Neotropical
biota related to the biota of other biogeographical areas?
Methodological approaches and the understanding of biogeographic patterns
were developed concomitantly, resulting in a wide variety of explanations to the
current distributional patterns of the Neotropical biota. During the 1850s and 1860s,
Joseph Hooker hypothesized the existence of intercontinental land bridges (e.g.,
between South America and Africa) and posteriorly changed his opinion and
accepted the idea of centers of diversity, agreeing with the dispersal views of
C. Darwin and A.F. Wallace (Llorente et al. 2000 ; Morrone 2007 ). Matthew’s ( 1915 )
work was the foundation for the, subsequently named, “New York School of
Zoogeography” (Croizat 1958 ; Morrone 2009 ), a school of thought reconciling bio-
geography, natural selection, and dispersal theories – a paradigm to neo-Darwinists.
In this context, dispersal explanations for distributional patterns state that ancient
species live in remote areas, whereas more recently derived species are located in
the centers of origin where they speciated. Even though dispersalism was not a uni-
ed research program, Simpson (
1940 ), Darlington ( 1957 ), and Mayr ( 1942 ) fol-
lowed W.D. Matthew’s ideas (Morrone 2002 ). Simpson ( 1940 ) proposed concepts
such as lter bridges and sweepstake routes , stating that any taxon can be originated
A. Ferrari et al.
65
in a center of origin and expands its distribution in every direction, until it reaches
an impassable barrier. Thus, the biota would have random distributions, because the
distribution of each taxon would be determined by its dispersal capabilities.
Panbiogeography was developed by L. Croizat to test dispersalist ideas. By com-
paring the distribution of plant and animal species, Croizat ( 1958 , 1964 ) found a
limited number of distributional patterns (Craw et al. 1999 ; Morrone 2007 ),
somewhat contrary to the dispersalist assumption of random distribution patterns.
Croizat’s work had either a low impact or was negatively criticized at its time
(Llorente et al. 2000 ).
The development of cladistics, providing rigorous means of recognizing groups
and its relationships and the wide acceptance of plate tectonics, promoted a shift on
biogeography, from dispersal, centers of origin, and identifi cation of subregions to the
establishment of areas of endemism and degrees of distributional concordance between
different taxa and the areas taxa occupy (Schuh and Slater 1995 ). Biogeographic
approaches became methodologically explicit only after Nelson and Platnick’s ( 1981 )
formalization of the cladistic biogeography method. The method’s assumption is that
there is evidence of shared common distributional patterns if congruence between
phylogenetic and biogeographic patterns of two or more taxa is found.
Biogeographic studies on Heteroptera face old and new impediments, such as
limited knowledge on phylogenetic relationship for most groups, limited taxon sam-
pling, lack of dating in phylogenetic hypotheses, and limited knowledge on the
distribution of taxa. Most biogeographical discussions are drawn from comparisons
between distributional patterns of studied taxa and other taxa, and geological infor-
mation. Also, biogeographical discussions frequently are neither based on phyloge-
netic information, nor dating nodes, nor on assumption of ancestral areas from
related fossils. Such approaches have serious methodological fl aws (Heads 2005 ),
because congruence or incongruence between non-dated biogeographical events
may be derived from pseudo-congruence or pseudo-incongruence patterns (Page
1990 ; Hunn and Upchurch 2001 ; Donoghue and Moore 2003 ).
A non-exhaustive overview of studies discussing the biogeography of Heteroptera
on the Neotropics, including those about intercontinental connections and local pat-
terns, is presented below. This section is intended as a starting point for new biogeo-
graphic studies on Heteroptera occurring in the Neotropics, facilitating literature
review, and is organized by infraorder. To avoid the fl aws exposed above, we do not
assume generalized patterns for the studies discussed.
3.3.1 Continental Biogeographical Connections
Gerromorpha
Andersen ( 1999 ) reviewed the phylogenetic, ecological, and geographical aspects of
species diversity of the Gerromorpha, fi nding that about 10 % of the 152 gerromor-
phan genera are marine and confi ned to the subtropical and tropical regions of the
world. According to Andersen, most marine water striders of the Neotropical region
3 Classifi cation and Biogeography of Neotropical True Bugs
66
have rather restricted distributional areas, such as the Rhagovelia ( Trochopus )
(Carpenter) (Veliidae) and Rheumatobates Bergroth (Gerridae), occurring in the
Caribbean and Pacifi c coasts of Central and South America, while other genera, such
as Husseyella Herring (Veliidae) and Telmatometroides Polhemus (Gerridae), are
confi ned to one of these two areas. The fauna of the Atlantic, Caribbean, and East
Pacifi c regions is mainly composed of marine lineages that most likely evolved mul-
tiple times from limnic ancestors. Andersen ( 1999 ) hypothesized that Darwinivelia
Andersen and Polhemus, Rheumatobates , and R. ( Trochopus ) evolved during the
Late Pliocene, before the emergence of the Isthmus of Panama. During the Cenozoic,
different shallow sea connections (e.g., Atlantic/Caribbean/East Pacifi c and Indo/
West Pacifi c) were available as dispersal routes for marine water striders and other
organisms occurring in the Pacifi c Ocean, the Tethys Sea, and Southern Africa.
Andersen ( 2000 ) described and discussed phylogenetic, paleontological, and
biogeographic aspects of eight gerromorphan species from Eocene Baltic amber.
Andersen hypothesized that these gerromorphan species seem to have their closest
living relatives either in the Palearctic region or in the Neotropical region or belong
to an ancestral lineage, which has left few living relict species in the Neotropical
region and on isolated islands of the Central Pacifi c.
Based on two putatively sibling genera, the South American Mesoveloidea
Hungerford and the West African Mesovelia Poisson, Andersen and Polhemus
( 2003 ) suggested mesoveliids have had an ancient, wide tropical distribution since
the Cretaceous and could, therefore, have diversifi ed in response to global tectonic
events. According to Andersen and Polhemus ( 2003 ), the restricted distributions of
many extant species may be an artifact of the lack of knowledge and sampling
effect. Andersen supports his hypothesis on the Neotropical genera Cryptovelia
Andersen and Polhemus, a monotypic genus known only to Brazil with an allied
species found in Borneo, and the Darwinivelia , described to contain a species found
on the Galapagos archipelago, with other species subsequently recorded from the
Atlantic and Pacifi c coasts of South America.
Polhemus and Polhemus ( 2008 ) reviewed the global diversity and taxonomic
richness of freshwater aquatic and semiaquatic Heteroptera (Gerromorpha,
Nepomorpha, and Leptopodomorpha). Modern gerromorphan lineages can be
traced back to the Mesozoic by fossil evidence and can be further supported from
Gondwanan distributions, assuming vicariant explanations (South America/Africa,
Platyvelia Polhemus and Polhemus / Angilia Stål (Veliidae); South America/
Australasia, Metrobates Uhler / Metrobatoides Polhemus and Polhemus (Gerridae)).
Based on their own and other colleagues studies, Polhemus and Polhemus ( 2008 )
assumed that the main areas of endemicity for aquatic Heteroptera in the world are (1)
Madagascar, (2) New Guinea, (3) Indochina, (4) the Malay Archipelago, (5) Australia,
(6) tropical Central and Western Africa, (7) the Guiana Shield of northern South
America, and (8) the Atlantic rainforests of eastern South America. The northern
South American Guiana Shield area is species-rich for aquatic Heteroptera, according
to Polhemus and Polhemus ( 2008 ) due to its ancient geological age, proximity to the
Equator, and topographic complexity. The Guiana Shield has many endemic species,
but still most of its genera occur in other areas of tropical South America.
A. Ferrari et al.
67
Leptopodomorpha
Before the work of Grimaldi et al. ( 2013 ), the Leptosaldinae (Leptopodidae) were
known from two Neotropical species, Leptosalda chiapensis Cobben, a fossil from
Mexican Miocene amber, and the extant Saldolepta kistnerorum Schuh and
Polhemus, from Ecuador and Colombia. Grimaldi et al. described two new fossil
species of Leptosalda Cobben from Miocene amber of the Dominican Republic and
a remarkable new fossil genus and species, Archaesalepta schuhi Grimaldi and
Engel, from Early Eocene Cambay amber from western India. They believe A.
schuhi is the sister taxon to the New World leptosaldines, suggesting leptosaldines
were more widespread and that their present-day distribution is relict. Their conclu-
sions should be taken cautiously, since the proposed relationships and biogeo-
graphic hypothesis are not based on a phylogenetic analysis.
Cimicomorpha
The understanding of Triatominae (Reduviidae) evolution still puzzles the knowl-
edge about its ancestral areas and its geographical distribution patterns. Trying to
answer some biogeographical questions, Schofi eld ( 1988 , 2000 ) proposed a poly-
phyletic origin of triatomines based on biogeographic arguments, with Asian fauna
being composed of at least two independent lineages (Hypsa et al. 2002 ). In a phy-
logenetic analysis of the New and Old World, including species of the Rhodniini,
Linshcosteini, and Triatomini (Reduviidae: Triatominae), Hypsa et al. ( 2002 ) found
confl icting results (dependent of rooting) for the origin of Triatominae, suggesting
either an origin in the northern areas of South America, in Central America, or in
southern North America. Hypsa et al. also found a clade of Asian species within the
Triatominae.
Studying the Tingidae sensu stricto in a phylogenetic framework, Lis ( 1999 )
erected the Cantacaderini to family status and applied Bremer’s ( 1992 ) ancestral
areas to explore its biogeography. The ancestral area of Cantacaderidae ( sensu Lis
1999 ) was smaller than the current distribution, included the Australian continent,
and the taxon probably originated around 140 million years ago (mya). Along a
dispersalist narrative, Lis ( 1999 ) argues that the sister taxa of the Neotropical genera
Stenocader Hambleton and Nectocader Drake are from New Zealand and Australia,
respectively, suggesting the Cantacaderidae colonization of the Neotropics via two
dispersal events through a connection between Antarctica and South America, about
50 mya. However, according to Guilbert ( 2012a ), the Vianaidinae (an exclusively
South American taxon) is sister to all other Tingidae, including the Cantacaderinae
(as a subfamily of Tingidae). This relationship hypothesis would imply that the com-
mon ancestor to Vianaidinae and Cantacaderinae could not be restricted to Australia,
but should rather have a Gondwanan distribution (Guilbert 2012b ). However, this
author agrees with Lis ( 1999 ) and Wappler ( 2006 ) that the Cantacaderinae colonized
the Neotropics by ancient vicariance followed by several recent dispersal events.
3 Classifi cation and Biogeography of Neotropical True Bugs
68
Pentatomomorpha
Based on evidence of Gondwanan origin to Aradoidea, Sweet ( 2006 ) proposed that
the Aradidae is an old taxon and its worldwide distribution most likely results from
vicariance. The Isoderminae (Aradidae) show an “Antarctic distribution,” occurring
in Chile, New Zealand, and Australia, while other subfamilies (Aradinae, Calisiinae,
Mezirinae, Carventinae, and Aneurinae) have cosmopolitan distributions, more
diverse in the tropics.
Mecidea Dallas comprises a group of stink bugs (Pentatomidae) occurring in
subtropical and adjacent temperate areas, apparently coinciding with xerophytic or
semi-xerophytic environments (Sailer 1952 ). To Sailer, Mecidea ’s distribution is
similar to countless taxa and is evidence of an ancient faunistic and fl oristic rela-
tionship between the semidesert and desert regions of the Mediterranean Basin,
South Africa, southern South America, and southwestern North America. According
to a dispersalist point of view, the Ethiopia, Eritrea, and Uganda highlands were
suggested as the center of distribution of Mecidea , because ve of the 14 species of
Mecidea occur in or are adjacent to this area.
Through Bremer’s ( 1992 ) ancestral area analysis, Lis ( 1999 ) suggests the
Cephalocteinae (Cydnidae) originated on the Indian continental block (as part of the
Gondwanaland) more than 125 mya. From the absence of paleontological data for
the taxa, he assumed that only migratory events could explain distribution patterns
and uses Gondwanan age for the group to substantiate the events of migration
between land masses without resorting to long-dispersal events.
Scaptocoris Perty (Cydnidae: Scaptocorini) reached the Neotropics through col-
onization from Antarctica, between 125 and 110 mya (Lis 1999 ); after, it radiated to
South America, giving rise to the endemic Atarsocori s Becker in Brazil and dispers-
ing to Central America. The distribution of the single species of Scaptocorini known
to Africa (Angola) was explained by dispersion of a “ Scaptocoris ancestral species,”
from South America to West Africa, and evolved into a separate genus, which dis-
played the same evolutionary trends in some characters as those in the South
American Atarsocoris .
3.3.2 Biogeography of the Neotropical Region
Enicocephalomorpha
Štys ( 2008 ) reviewed the geographic distribution of the unique-headed bugs’ genera
of Aenictopecheidae and Enicocephalidae, emphasizing distributional patterns
based on zoogeographic regions. According to Štys, the proposition of historical
biogeography hypotheses for the group would be premature, given the lack of
knowledge for some faunas, particularly of the islands and archipelagos of the
Atlantic and Indian Oceans, and the lack of phylogenies at the generic level.
A. Ferrari et al.
69
Five enicocephalomorphan genera have been described for the Neotropical
region, occurring from the Caribbean islands and southern Mexico to as south as the
Tucuman province and Santa Catarina state, in Argentina and Brazil, respectively.
Of these genera, four are assigned to the Enicocephalidae and one to the
Aenictopecheidae. About 40 unique-headed bug species have been described to the
Neotropical region, but it is estimated that at least 100 more have yet to be described
(Štys 2008 ). Additionally, a monotypic genus, Gamostolus Bergroth
(Aenictopecheidae), occurs on the South American Subantarctic region in southern
Chile (Magallanes and Osorno provinces) and Argentina (Staten Island).
Gerromorpha and Nepomorpha
Based on track analysis of 60 species of Belostomatidae, Corixidae, Micronectidae,
and Gerridae from Chaco province, Morrone et al. ( 2004 ) found fi ve generalized
tracks and three panbiogeographic nodes: Tracks include (1) Bolivia and northwest-
ern and central Argentina (11 spp.); (2) southern Brazil, eastern Bolivia, Paraguay,
and northeastern Argentina (four spp.); (3) southeastern Brazil and northeastern
Argentina (eight spp.); (4) southeastern Brazil, Uruguay, and central western
Argentina (fi ve spp.); and (5) southern Argentina (three spp.). Nodes include (1)
northeastern Argentina, (2) central Argentina, (3) and central south Argentina. The
authors stated that the Chaco province appears to be a natural biogeographical area
that shares taxa with the Amazonian, Parana, and Patagonian biogeographic
provinces.
Leptopodomorpha
Trying to answer whether the Andean distribution of Pseudosaldula (Saldidae) is
part of a broader Austral distributional pattern (including New Zealand, Australia,
and part of Antarctica), Schuh and Polhemus ( 2009 ) discuss the genus’ biogeogra-
phy based on a morphological phylogenetic hypothesis. Using a qualitative approach
to analyze the genus’ distribution, they recognized fi ve areas of endemism: Northern
Andes, Northern Peru, Puna, Central Chile, and Subantarctic. Using two different
cladograms obtained by different optimization criteria (equal weights and implied
weighting), area cladograms were constructed, and they found either the Northern
and Southern Andes being commingled or a great hierarchical structuring of the
Andes, with southern areas basal on the cladogram. The following hypothesis for the
biogeography of the group, is proposed ( sic Schuh and Polhemus 2009 ): (1)
Subantarctic is the basal area on the cladogram; (2) Central Chile is the next area on
the cladogram, and either P. penai Schuh and Polhemus or P. pilosa Schuh and
Polhemus are endemic to it; (3) Puna is the next area on the cladogram; and (4)
Northern Peru and Northern Andes are sister areas.
3 Classifi cation and Biogeography of Neotropical True Bugs
70
Cimicomorpha
Neotropical species of Rahasus Amyot and Serville (Reduviidae: Peiratinae) and
other three related genera ( Eidmania Teuber, Melanolestes Stål, and Thymbreus
Stål) were studied by Morrone and Coscarón ( 1998 ), using a cladistic biogeographic
approach. General area cladograms were constructed using two methods (Component
2.0 by Page 1993 and paralogy-free subtree, Nelson and Ladiges 1996 ) and resulted
in scenarios previously proposed by Morrone and Coscarón ( 1996 ): “open
vegetated” provinces (Desierto, Caatinga, Cerrado, and Chacoan), found basally on
the trees, and “forest” provinces (Caribbean, Amazonian, Paraná, and Atlantic). The
general area cladogram was in agreement with the previous scenario proposed by
Morrone and Coscarón ( 1996 ) and resulted in “open vegetated” provinces (Desierto,
Caatinga, Cerrado, and Chacoan) at the base, whereas the “forest” provinces
(Caribbean, Amazonian, Paraná, and Atlantic) formed a group. Morrone and
Coscarón (1998) relate the formation of the South American arid diagonal with the
uplift of the Andes and hypothesized it as a vicariant event that separated the for-
ested areas into two portions (Caribbean + Amazonian and Paranaense + Atlantic)
during the middle Miocene. This can be considered one of the most comprehensive
cladistic biogeography analyses searching for general patterns on Neotropical
Heteroptera.
Abad-Franch and Monteiro ( 2007 ) presented an approximation to the historical
biogeography and evolution of the main triatomine lineages ( Panstrongylus Berg
and Triatoma Laporte) that occur in the greater Amazon. They found the distribu-
tional pattern of the Rhodniini in the Amazon forest to be associated with two bio-
geographically well-defi ned groups of species (“ pictipes group” and “ robustus
group,” with trans- and cis-Andean distribution, respectively), invoking a basal
evolutionary split within the tribe in this area. The origin of Amazonian triatomine
species was suggested to be associated with historical, ecological, and anthropo-
genic ecological disturbances.
Paula et al. ( 2007 ) proposed a biogeographic hypothesis to species of Rhodniini
(Reduviidae: Reduviinae), based on the historical background of the Neotropical
region proposed by Amorim ( 2009 ). The authors employed a reconciled tree
method to deduce taxon-area associations, implemented in TreeMap (Charleston
and Page 2001 ). Twelve optimal solutions were found to explain Rhodniini bio-
geographical scenarios, with six vicariance events, 20 duplications (sympatry), at
least three dispersals, and one extinction event. However, Paula et al. ( 2007 )
decided not to use any of these reconstructions, instead opting to discuss specifi c
scenarios for some lineages that are not necessarily present in all optimal solu-
tions. The main events evoked to explain biogeographic patterns of the group are
the uplift of the Central Andes and Andes breakup into three separate cordilleras,
emergence of the Isthmus of Panama, and uplift of the Serra do Mar and Serra da
Mantiqueira (Brazil). The lack of resolution in the biogeographical history of the
group may be the result from poor taxon sampling and inappropriate areas
included in the study.
A. Ferrari et al.
71
The bee assassin crassipes and pictipes species groups of Apiomerus Hahn
(Reduviidae: Harpactorinae) were studied by Berniker and Weirauch ( 2012 ). They
used the phylogeny to explore biogeographic patterns of 12 species and determine
the boundary between Nearctic and Neotropical areas of endemism. Their results
support the limits between the Neotropical and Nearctic regions along the Isthmus
of Tehuantepec (Mexico), congruent with previous biogeographical analyses for
New World insects (e.g., Halffter 1987 ; Morrone and Marquez 2001 ). Under a
Brooks’s parsimony analysis (BPA), Berniker and Weirauch ( 2012 ) corroborate the
relationship between Chiapan-Guatemalan Highlands, Talamancan Cordillera, and
northwest South American areas and together are sister to the remainder of the
Neotropics; this pattern was found by previous studies, such as Amorim and Pires
( 1996 ) and Amorim ( 2001 ). However, this assertion must be taken cautiously, since
the authors did not use a BPA area classifi cation with the intent of testing the
assumptions of Amorim and Pires ( 1996 ) of an Amazonia composed of two distinct
biotic components.
Pentatomomorpha
Brochymena Amyot and Serville and Parabrochymena Larivière are the only repre-
sentatives of Halyini (Pentatomidae: Pentatominae) occurring in the New World:
Brochymena all over North and Central America between 50°N and 15°N and
Parabrochymena only in the eastern United States, southeastern Canada, and
Central America. Generally, Larivière ( 1994 ) explains the distribution of both gen-
era based on major geological events and ecological aspects of North America,
particularly assumptions concerning climate change. Under a dispersalist frame-
work, he asserts that areas of greatest diversity of Brochymena and Parabrochymena
correspond well with areas occupied by hypothesized oldest lineages of the genera.
He speculates there is a general trend of diversity reduction towards northern lati-
tudes, perhaps due to Pleistocene glaciation, but also pinpoint there is an overall
pattern observed in pentatomids to not extend far beyond warm temperate
conditions.
Grazia ( 1997 ) explored the biogeographical relationships of the Evoplitus genus
group ( Evoplitus Amyot and Serville, Pseudevoplitus Ruckes, and Adevoplitus
Grazia and Becker; Pentatomidae: Pentatominae). Evoplitus occurs on the Atlantic
Forest, including Paraguay and northern Argentina, and its sister group,
Adevoplitus + Pseudevoplitus , is distributed in Central America, northern Colombia,
and eastern Venezuela and Amazonian Basin. The contact zone between the two
clades is along the Amazonas, Madeira, and Mamoré rivers. Under the same reason-
ing employed by Grazia ( 1997 ), the biogeography of the Neotropical Brachysthetus
Laporte was studied by Barcellos and Grazia ( 2003 ). In both works, the authors fi nd
distributional patterns congruent with the hypotheses of Amorim and Pires ( 1996 )
and Amorim ( 2001 ) of two distinct Amazonias, the formation of an epicontinental
sea in the Maracaibo region, after the Late Cretaceous separated an area in
Mesoamerica from the remaining Amazonian elements.
3 Classifi cation and Biogeography of Neotropical True Bugs
72
Fortes and Grazia ( 2005 ) and Simões et al. ( 2012 ) studied Serdia Stål
(Pentatomidae: Pentatominae), a Neotropical genus distributed from Costa Rica to
southern Brazil and northern Argentina, with highest diversity in southern and
southeastern Brazil. Reanalyzing the morphological matrix of Fortes and Grazia
( 2005 ), Simões et al. ( 2012 ) proposed biogeographic hypotheses to Serdia based on
vicariance analysis (Hovenkamp 1997 , 2001 ), which consists of fi nding the disjunct
(allopatric/vicariant) distributions in the nodes of the cladogram. They identifi ed
three nodes sharing disjunct distributions, which might be associated to vicariant
events related to the development of the Chacoan subregion (Morrone 2006 ) that,
during the Paleogene and Neogene (former Tertiary), divided the once continuous
Amazonian-Parana Forest.
The ancestral area of Schraderiellus group (Pentatomidae: Discocephalinae) is
the Amazonian subregion, from where the species successively dispersed (Campos
and Grazia 2006 ). The southern distributional limits of the Schraderiellus group,
the Amazonas, Madeira, and Mamoré river basins, can also be explained by the
independent evolution of biota from the northwest and southeast of Amazonia
proposed by Amorim ( 2001 ). The Schaefferella group (Pentatomidae:
Discocephalinae), widely distributed in Central and South Americas, is believed to
have originated in the Paraná subregion with further expansions to the north, towards
southeastern Amazonian subregion, and to the south, towards the Chacoan
subregion. The distributions of Uvaldus Rolston and Clypona Rolston (Pentatomidae:
Discocephalinae), restricted to the Araucaria Forest and Chaco, respectively, could
be the result of vicariant events separating the Parana and Chacoan subregions.
Procleticini (Pentatomidae: Pentatominae) is a small tribe (about 30 species in
11 genera) found only in the New World. According to Bernardes et al. ( 2009 ), the
group Lobepomis Berg + Neoderoploa Pennington + Procleticus Berg and basal spe-
cies of Thoreyella Spinola are restricted to open vegetation formations of Neotropical
region (the Chacoan subregion), and the most apical Thoreyella species are more
related to forested habitats in the Parana Forest subregion.
3.3.3 Distributional Patterns of Neotropical Heteroptera
Recently, studies of distribution patterns within Heteroptera have increased but are
still largely biased towards better-known taxa. In most of those studies, authors point
out to the lack of phylogenetic hypotheses and outdated phylogenies for the group
and stress their studies are early approaches to the understanding of distributional
patterns of the taxa. Macroecological and biogeographic aspects of Heteroptera are
hampered from being further understood because of the lack of accessible online
databases of biological collections and more research on phylogenetic relationships.
One of the best studied groups of Heteroptera is the Triatominae (Reduviidae).
The group has been employed in macroecological studies in attempts to understand
its richness and distribution patterns on the Neotropics (e.g., Rodriguero and Gorla
2004 ; Diniz-Filho et al. 2013 ; Fergnani et al. 2013 ).
A. Ferrari et al.
73
Rodriguero and Gorla ( 2004 ) examined how New World Triatominae species
richness responds to latitudinal gradients and explored the relevance of geographi-
cal area and available energy. Based on the distribution of 118 triatomine species,
the authors found for the fi rst time in obligatory hematophagous organisms an
evident increase in the number of species of Triatominae from higher to lower
latitudes. Such a pattern is not expected to insects (Rodriguero and Gorla 2004 ), but
is found in some mammalian taxa. Habitable area effect on species richness is dif-
ferent in each hemisphere: on the Southern Hemisphere, an increase in species
richness is correlated with an increase in habitable area from the poles towards the
Equator, whereas on the Northern Hemisphere, there is an increase of species rich-
ness towards low latitudes; habitable area does not affect this relationship. There is
a signifi cant correlation of species richness with habitable area, mainly in the
Southern Hemisphere and eastern longitudes.
Diniz-Filho et al. ( 2013 ) tested different environmental hypotheses to understand
geographical patterns of richness and the distribution of 115 Neotropical triatomine
species. Testing seven different hypotheses of climatic effects as drivers of species rich-
ness, using spatial eigenvector mapping and nonspatial ordinary least squares multiple
regression models, they found water, energy, temperature, and temperature seasonality
to be the environmental variables with relatively higher explanatory power of species
richness and elevation variables having minor effects. The unique effects of these vari-
ables are quite diffi cult to disentangle because of the collinearity among variables and
residual autocorrelation and may also be due to low taxonomic sampling.
Fergnani et al. ( 2013 ) conducted a complementary study to understand large-
scale spatial patterns of morphological diversity and species richness of triatomine
species in terms of environmental gradients. Studying 91 species and 12 morpho-
logical attributes of Neotropical triatomine, they found the latitudinal gradient of
species richness to be in agreement with previous studies (Rodriguero and Gorla
2004 ; Diniz-Filho et al. 2013 ). The morphological diversity, by means of Gower
index, also followed a latitudinal gradient, suggesting an overall spatial congruence
between species richness and morphological diversity. However, the overall correla-
tion pattern between species richness and morphological diversity is not homoge-
neous throughout taxon distribution (e.g., Brazil and Argentina have regions of high
species diversity, but low morphological diversity). According to Fergnani et al.
( 2013 ), their’s was the fi rst study where this kind of relationship was demonstrated for
insects on a continental scale, demonstrating that for the Triatominae, species rich-
ness and morphological diversity cannot be considered substitutes for one another.
One of the few studies that looked for distribution patterns exclusively on
Neotropical Pentatomidae (Hemiptera) was done by Ferrari et al. ( 2010 ), analyzing
the distribution of 222 species belonging to 14 genera using analysis of endemicity
(NDM – Szumik et al. 2002 ; Szumik and Goloboff 2004 ) and identifying hierarchi-
cal endemic areas in the Atlantic Forest. The Amazonian region was identifi ed as a
single area on the consensus, its southeastern portion share elements with the
Chacoan and Paraná subregions, while the Cerrado and the Caatinga were not iden-
tifi ed as unique areas of endemism.
3 Classifi cation and Biogeography of Neotropical True Bugs
74
3.3.4 Phylogeography
Almost 30 years after Avise et al. ( 1987 ) coined the term phylogeography, two
major papers reviewed the subject, including works dealing with the Neotropics. As
emphasized by Beheregaray ( 2008 ), out of the 3049 phylogeographic papers pub-
lished around the world until 2006, only 15 % explored Southern Hemisphere
organisms; the numbers are even lower if we consider only published articles about
terrestrial invertebrates on South America (8 % out of 313 papers). Focusing on
South America, Turchetto-Zolet et al. ( 2013 ) indicate that, from 1987 to 2011, only
29 studies on invertebrates were published, most emphasizing in vectors of human
diseases, such as Chagas disease (Hemiptera: Reduviidae) and malaria (Diptera:
Culicidae). When compared to other biogeographical regions and continents, phy-
logeographical studies in South America are still incipient, the same happening in
the rest of the Neotropical Region.
The rst effort on phylogeography of Heteroptera was populational studies about
species of economic or medical importance (e.g., Monteiro et al. 1999 ; Sosa-Gomez
et al. 2004 ), triggering studies which focused on Triatominae vectors of Trypanosoma
cruzi (Chagas), a parasitic euglenoid protozoan that causes Chagas disease. The
Triatominae (Reduviidae), known as kissing bugs due their hematophagous feeding
habit, are distributed from Argentina to the United States, between the latitudes
46°S and 46°N (García et al. 2013 ). Of the 15 known genera of Triatominae, 14
occur in the New World (Gourbière et al. 2012 ), and almost all of the 145 species
recognized for Triatominae (Gonçalves et al. 2013 ) seem to be potential vectors of
trypanosomatids. Three species are of greatest epidemiological relevance: Triatoma
infestans Klug, Triatoma brasiliensis Neiva, and Triatoma dimidiata (Latreille).
Triatoma infestans is the most studied species because, alone, it is responsible
for half of the Chagas disease cases in the Neotropics. The evolutionary lineage of
T. infestans originated between 2.7 and 1.0 mya as a derivation from T. platensis
Neiva (Bargues et al. 2006 ). Bargues et al. ( 2006 ) suggest T. infestans originated
from Bolivian highlands, and the current lineages allows the identifi cation of clear
differences between Andean and non-Andean populations. Two initial dispersal
routes of T. infestans were hypothesized, one through the Andean highlands of
Bolivia and Peru and another through the lowlands of Argentina, Paraguay, Uruguay,
Brazil, and Chile. Both these primary lineages are corroborated by independent
nuclear, mitochondrial, and multilocus microsatellite studies (Monteiro et al. 1999 ;
Piccinali et al.
2009 ; Pérez-de-Rosas et al. 2011 ). Torres-Pérez et al. ( 2010 ) sug-
gested that T. infestans would have originated outside of Bolivia, but they also rec-
ognized the Andean and non-Andean lineages with estimated divergence time
around 0.388–0.588 mya, agreeing globally with the estimate dates found by
Bargues et al. (
2006 ). On the other hand, the widespread distribution of T. infestans
in South America is attributed to its domiciliation, a probable recent event following
the New World colonization by humans around 12,000 years ago (González-José
et al. 2003 ) and main range expansion in post-Colombian times, after the seven-
teenth century until today (Panzera et al. 2004 ).
A. Ferrari et al.
75
It is believed that the contemporary population structure has been dramatically
infl uenced by human-vector interactions, as indicated by the complex biogeographic
pattern of T. infestans , at both local and regional scales (Torres-Pérez et al. 2010 ).
The relationship between human dwellings and T. infestans has elicited studies aim-
ing to understand: insecticide effectiveness through haplotype diversity/persistence,
the fi ne-scale migration ability, offspring viability between populations/morphs,
capability of house infestation, and reinfestation of sylvatic and peridomestic
populations (e.g., Marcet et al. 2008 ; Pérez-de-Rosas et al. 2008 , 2013 ; Piccinali
et al. 2009 , 2011 ), as resources for developing rational vector control strategies
(Piccinali et al. 2009 ).
In Northeastern Brazil, T. brasiliensis is the most important Chagas disease vec-
tor. Monteiro et al. ( 2004 ) analyzed the populations of T. brasiliensis across its
distribution and indicated that each chromatic form is genetically different from
each other, suggesting the existence of a species complex: the forms juazeiro ,
melanica , and brasiliensis + macromelasoma should be treated as separate species.
Nowadays, T. juazeirensis Costa & Felix and T. melanica Neiva & Lent are consid-
ered species of the T. brasiliensis complex. The population structure of brasiliensis
does not show strong geographic segregation, suggesting recent range expansion.
The divergence time between brasiliensis and melanica is estimated to have
occurred around 5.2 mya, which would place their common ancestor in the early
Pliocene. On the other hand, brasiliensis + macromelasoma population structure
does not show strong geographic segregation, suggesting recent range expansion.
Triatoma dimidiata is the main vector of T. cruzi throughout Central America to
Ecuador. The diversity of habitats explored by T. dimidiata involves domestic and
peridomestic dwellings and non-domiciliated and sylvatic populations, act as
sources of reinfestation. Along the distribution of T. dimidiata , some populations/
subspecies are suggested by phenotypical, genotypical, and ethological traits.
Bargues et al. ( 2008 ) analyzed its intraspecifi c variability, fi nding high haplotypic
diversity supporting three groups: group 1, widespread (Colombia, Ecuador,
Guatemala, Honduras, Mexico, Nicaragua, and Panama) and highly variable; group
2, geographically restricted to Guatemala and Mexico; and group 3, occurring in
Guatemala, Honduras, and Mexico. The high haplotypic variability found in T.
dimidiata seems to be remarkably outside the limits of the intraspecifi c variability
range known for Triatoma species (Bargues et al. 2008 ; Monteiro et al. 2013 ).
Monteiro et al. ( 2013 ) refi ned the analyses of Bargues et al. ( 2008 ) by adding
different molecular markers and fi nding four genetic groups for T. dimidiata . Both
groups of authors found a complex of monophyletic cryptic species including the
subspecies of T. dimidiata plus T. hegneri Mazzotti. The Triatoma dimidiata species
complex is believed to have originated 5.9–10.5 mya. Hypotheses to each popula-
tion/subspecies origin, expansion, and distribution are explored on the literature
(Bargues et al. 2006 ; Monteiro et al. 2013 ; Gómez-Palacio and Triana 2014 ) and
include distributional expansions by relatively recent human activity, mountain
uplifts, and the connection of South and North Americas through the Isthmus of
Panama during the Pliocene (3–5 mya).
3 Classifi cation and Biogeography of Neotropical True Bugs
76
Other Neotropical reduviid genera have been studied under phylogeographical
approaches. On the Amazonian region, the phylogeography of Rhodnius prolixus
Stål and R. robustus Larrousse was studied by Monteiro et al. ( 2003 ), sampling in
seven Latin American countries. Five clades were found, being R. prolixus homoge-
neous. Rhodnius robustus is represented by four paraphyletic clades, one of them
( R. robustus Clade I) more closely related to the R. prolixus clade. The R. prolixus
and R. robustus Clade I is believed to have originated around 1.4 mya, when an
ancestral stock was spread in different refugia at the Orinoco lowland forest
(Venezuela). The other R. robustus clades are from the Amazon forest region.
Extremely low nucleotide diversity of R. prolixus suggests a recent bottleneck and
posterior dispersion facilitated by human activity. The clade R. prolixus + R. robus-
tus senso lato suggests an origin in between 3.7 and 2.4 mya. Dating within the
Pleistocene, the pattern of phylogenetic discontinuity with geographical distribution
of haplotypes could involve long-term biogeographical barriers to gene fl ow (Avise
et al. 1987 ) and could be explained by the refugium theory (Monteiro et al. 2003 ).
Maia-da-Silva et al. ( 2007 ) compared the phylogeny of Rhodnius with
Trypanosoma rangeli Tejera, 1920 populations, showing a signifi cant overlap in
the distribution and demographic correspondence between the Rhodnius spp. and
T. rangeli lineages. The pattern is consistent with a hypothetical long parasite- vector
coexistence with and is supported by a high congruence between the phylogeo-
graphical analysis of both T. rangeli lineages and Rhodnius species.
Mepraia Mazza, Gajardo, and Jörg, comprised by three species, is an important
endemic Chilean vector of T. cruzi in the sylvatic cycle. Campos et al. ( 2013 ) found
three lineages of Mepraia , congruent with the current recognized species. All popu-
lations tested were highly structured, suggesting that they have not been affected by
strong bottlenecks and/or experienced sudden demographic changes due to repeated
climatic fl uctuations. The origin of Mepraia is suggested to have occurred around
3.6 mya, during the pre-Pleistocene. Mepraia spinolai (Porter) is recognized as the
oldest lineage, followed by M. gajardoi Frias, Henry, and Gonzales (originating
0.99 mya) and M. parapatrica Frías-Lasserre (originating 0.66 mya).
The southern green stink bug Nezara viridula (L.) (Pentatomidae) is a polymor-
phic and worldwide pentatomid pest, causing economic damage to many crops
(Panizzi et al. 2000 ). To elucidate its origin and dispersion routes, Karvar et al.
( 2006 ) sampled specimens from four continents (Africa, America, Europe, and
Asia), and Li et al. ( 2010 ) added populations from China and Iran, both agreeing in
a basal phylogeographic position of N. viridula from Africa and suggesting a deep
division between African and non-African populations. Using different molecular
clocks, Karvar et al. ( 2006 ) suggested the division of African and non-African popu-
lations of N. viridula since the Pliocene, while Li et al. ( 2010 ) suggested the split
during the Miocene. Both groups of authors concluded that the New World popula-
tions of N. viridula are more closely related to European populations. Karvar et al.
( 2006 ) hypothesize different routes for the American colonization: one from the
eastern Mediterranean (Greece, Italy) to Central America and from there to eastern
United States and the western coastal areas of South America and another originat-
A. Ferrari et al.
77
ing in the western Mediterranean (Iberian Peninsula) and dispersing to the eastern
coastal areas of South America. The relationships among Neotropical populations
should be better investigated, as well as recent human activity-mediated dispersion.
As showed above, most phylogeographic studies are biased to species with medi-
cal relevance and economic impact, and the aim of these studies are often inter-
twined with applied interests. Nevertheless, as side results, speciation hypotheses,
taxa coalescence, population demography, and geographical processes have been
improved to those taxa on the Neotropical region. Furthermore, the integrative
nature of phylogeography and increased access to molecular evidences are helping
elucidate intraspecifi c relationships, infl uencing phylogenetic hypotheses and taxo-
nomic decisions.
Phylogeographic studies on the Neotropics are incipient, especially to terrestrial
invertebrates (Turchetto-Zolet et al. 2013 ), and most Neotropical biomes, such as
the Amazonia, Cerrado, Atlantic Forest, Pampa, and Caribbean islands, are poorly
known. The current systematic, ecological, and distributional knowledge about
Neotropical heteropterans make them a useful source to phylogeography. The phy-
logeography could support the identifi cation of refugia and contact zones, enlight-
ening the biogeographical processes and improving the understanding of lineages
history and processes of diversifi cation.
3.4 Concluding Remarks
Much remains to be studied regarding the systematics and biogeography of
Heteroptera, especially on the Neotropics. Despite the high diversity of true bugs,
most families occurring in the Neotropical region are neglected. In fact, the best
known taxa are those of economical or medical importance (e.g., Reduviidae,
Pentatomidae), although Pentatomidae lacks an updated Neotropical catalog. In the
last decades, though, the training of new systematists has improved the knowledge
on some families, as will be presented in the following chapters. However, it is time
to expand the scope of revisionary, systematic, and biogeographic studies.
There is a general and global lack of phylogenetic studies for Neotropical taxa,
especially with those taxa of broad taxonomic coverage and consistent out-group
sampling. The search for heteropteran biogeographic patterns is hampered by the
lack of phylogenies and a clear use of biogeographic methodologies. Phylogeographic
studies are incipient, focused on taxa of economic importance, even though the
integrative nature of the subject can help elucidate the evolutionary history on the
Neotropics.
Overall, future works should incorporate new techniques for data gathering and
new methodologies for data analysis and become taxonomically broader and com-
prehensive. All of it would facilitate the understanding of the evolutionary history of
the different groups.
3 Classifi cation and Biogeography of Neotropical True Bugs
78
Acknowledgments We thank M. Guidotti (UFRGS) for his help with the Cimicomorpha phylo-
genetic section, the fi nancial support from the Conselho Nacional de Desenvolvimento Científi co
e Tecnológico (CNPq) (Ed. Universal 470796/2012-0), a postdoctoral fellowship from the
Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) to A. Ferrari (PNPD
02637/09-0 and CAPES/FAPERGS 07/2012), and doctoral fellowships to K.R. Barão (CNPq
142447/2011-0, CAPES/PDSE BEX5641/13-6) and F.M. Bianchi (CAPES/PDSE), and research
fellowships from CNPq to J. Grazia and L.A. Campos are also greatly acknowledged.
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3 Classifi cation and Biogeography of Neotropical True Bugs
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... Las relaciones filogenéticas de la subfamilia Vianaidinae en la actualidad no están del todo claras (Guilbert et al., 2014). La gran mayoría de autores parecen estar de acuerdo en que es un grupo hermano del resto de todos los Tingidae (Schuh y Štys, 1991;Schuh et al., 2006Schuh et al., , 2009Guilbert, 2012;Ferrari et al., 2015;Guidoti y Montemayor, 2016) y consideran, por tanto, que tiene rango de subfamilia. Pero otros autores consideran que su rango es el de familia (Kormilev, 1955;Štys y Kerzhner, 1975;Froeschner, 1996Froeschner, , 1999Golub y Popov, 2000, 2003Zhang et al., 2005;Montemayor y Carpintero, 2007;Montemayor, 2014). ...
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... Robust phylogenetic hypotheses are key to the advancement of comparative studies addressing questions in different fields of life sciences, such as evolutionary biology and ecology. The first hypothesis of phylogenetic relationships for the Heteroptera (Hemiptera) explicitly employing cladistic methods was developed by Schuh (1979) (for a historical overview see Weirauch & Schuh, 2011;Ferrari et al., 2015). Since then, phylogenetic hypotheses have been produced for higher-level taxa of Heteroptera based on either morphological (Mahner, 1993) or molecular data (Xie et al., 2008), or both data sources combined (Wheeler et al., 1993). ...
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