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Absence asymmetry: the evolution of monorchid beetles (Insecta: Coleoptera: Carabidae).

TL;DR: No function conclusively explains the ontogenetic loss of one testis in these carabid beetles, but it is tentatively suggested that testis loss is driven wholly by an interaction among the internal organs of these beetles, possibly due to selective pressure to maximize the comparatively large accessory glands found in these taxa.
Abstract: Asymmetrical monorchy, or the complete absence of one testis coupled with the presence of its bilateral counterpart, is reported for 174 species of the carabid beetle tribes Abacetini, Harpalini, and Platynini (Insecta: Coleoptera: Carabidae) based on a survey of over 820 species from throughout the family. This condition was not found in examined individuals of any other cara- bid beetle tribes, or of other adephagan beetle families. One monorchid taxon within Platynini exhibits symmet- rical vasa deferentia at the beginning of the pupal sta- dium, suggesting that developmental arrest of the under- developed vas deferens takes place in pupation. The point at which development of the testis is interrupted is un- known. Complete absence of one organ of a bilateral pair—absence asymmetry—is rarely found in any animal clade and among insects is otherwise only known for tes- tes in the minute-sized beetles of the family Ptiliidae, ovaries in Scarabaeinae dung beetles, and ovaries of some aphids. Based on current phylogenetic hypotheses for Carabidae, testis loss has occurred independently at least three times, and up to five origins are possible, given the variation within Abacetini. Clear phylogenetic evidence for multiple independent origins suggests an adaptive or functional cause for this asymmetry. A previously posited taxon-specific hypothesis wherein herbivory in the tribe Harpalini led to testis loss is rejected. Optimal visceral packing of the beetle abdomen is suggested as a general explanation. Specifically, based on the function of various organ systems, we hypothesize that interaction of internal organs and pressure to optimize organ size and space usage in each system led to the multiple origins and main- tenance of the monorchid condition. Testes are the only redundant and symmetrically paired structures not thought to be developmentally linked to other symmetri- cal structures in the abdomen. Among all possible organs, they are the most likely—although the observed frequency is very small—to bypass constraints that maintain bilat- eral symmetry, resulting in absence asymmetry. However, based solely on our observations of gross morphology of internal organs, no function conclusively explains the on- togenetic loss of one testis in these taxa. Unlike the anal- ogous absence asymmetry of organs in other animal groups, no dramatic body-form constraint— e.g., snakes and lung loss, ptiliid beetles' small body-size and rela- tively giant sperm— or adaptive scenario of improved lo- comotory performance— e.g., birds and ovary loss due to flight constraints—applies to these carabid beetles. We tentatively suggest that testis loss is driven wholly by an interaction among the internal organs of these beetles, possibly due to selective pressure to maximize the com- paratively large accessory glands found in these taxa. However, as the ordering of these evolutionary events of testis loss and accessory gland size increase is not known, large accessory glands might have secondarily evolved to compensate for a decreased testicular output. J. Morphol. 000:000 - 000, 2005. © 2005 Wiley-Liss, Inc.

Summary (3 min read)

Introduction

  • Interaction among the internal organs of these beetles, possibly due to selective pressure to maximize the comparatively large accessory glands found in these taxa.
  • In this article the authors describe the phylogenetic distribution of monorchy and discuss its evolution.
  • The absence asymmetry of testes in carabid beetles is therefore a unique type of evolutionary loss among bilateral animals.

Carabidae

  • Among the families of the coleopteran suborder Adephaga, Carabidae, with nearly 40,000 species (Lorenz, 1998), is the most diverse.
  • Enough is known about the monophyly of groups that include monorchid taxa to propose minimal numbers of origins of the trait.
  • Both Smrž (1981) and their study confirm that those taxa have only one single follicle testis.
  • Accessory glands are quite various in insects and have been studied in many taxa (Chen, 1984; Gillott, 2003).

MATERIALS AND METHODS

  • Specimens were collected and either maintained alive, preserved in EtOH (90% or greater), Pampel’s or in Kahle’s fluid (Barbosa, 1974).
  • Ethanolpreserved specimens were dissected in 95% and other preserved material under 70% EtOH.
  • Alternatively, images were taken using a digital camera and drawings made as an overlay using standard image editing software.
  • Emphasis was placed on sampling species and genera within the monorchid tribes and in groups thought to be closely related to them.

RESULTS General Description of Male Carabid Reproductive Tract

  • Except as noted below, the carabid male reproductive system is quite typical of insect reproductive organs.
  • The ejaculatory duct (ed) emerges from the foramen of the sclerotized median lobe and ramifies anteriorly into two tubular accessory glands (ag).
  • The four types of accessory glands the authors recognize here (Fig. 2) are based only on published illustrations and material dissected by KWW, and do not include all species known for testis condition.
  • The simple form (Fig. 2C), which consists of two paramedial, tomaculate-form glands, is found in many taxa including basally divergent carabids and much more highly derived (Lebiini, Lachnophorini, Zuphiini) members of Harpalinae.
  • They are generally oval or pyramidal in form (Fig. 5) and their shape may be defined by adjacent organs, e.g., accessory glands or gut.

DISCUSSION

  • There is no other character supporting monophyly of a group consisting of only the monorchid carabids (Harpalini, part of Platynini, and part of Abacetini).
  • Until a much more comprehensive study of the relationships within abacetine-like taxa is undertaken, it is not possible to determine whether the two monorchid states (right testis absent, left testis absent) in Fig.
  • Harpalini is apparently an isolated taxon that primitively evolved the monorchid condition and has subsequently diversified.
  • A second group of diorchid taxa have been classified as Platynus subgenus Batenus (Liebherr, 1989) (Table 1).
  • The presence of equally developed, although small, vasa deferentia in the pupa of the monorchid platynine taxon Blackburnia erro (Table 1) establishes that testis and the associated vas deferens asymmetry progressively develops during the pupal stage.

Transformation to Monorchy

  • Within ptiliid beetles, the single, medial testicular mass of Nossidium pilosellum appears to be an intermediate condition between diorchy and possession of a single lateral testis.
  • All organ systems located in the abdominal cavity must “compete” for space, for an increase in one system can only be accommodated by stretching intersclerotic membranous cuticle, or shrinking another system.
  • 469) suggested that the “exceeding development” of the gut—an adaptation to herbivory—as the selective pressure that led to degeneration of the left testis in Harpalini, also known as Smrž (1981.
  • The accessory glands in male carabid beetles, particularly in monorchid taxa, appear to occupy a large portion of the abdominal volume.
  • The authors comparative sample shows that testes are much more variable in size, shape, and position in carabids with sinuate accessory glands than in carabids with simple or mirror-recurved glands, suggesting that these structures are directly impacting testis development.

Why Testes Are Lost

  • If limited space for the viscera is causing absence asymmetry, an explanation is still needed for why a testis would be lost rather than some of the other structures in the abdomen.
  • Similarly, the gut, including Malpighian tubules, is based on and functions as a bilaterally symmetrical structure.
  • The female internal tract is rarely symmetrical, with the bursa dramatically asymmetrical and the accessory gland and spermatheca directed to the left or right (Liebherr and Will, 1998; Will, 2002).
  • In all of these possible mating systems an increase in accessory gland ejaculate could lead to avoidance of direct sperm competition, reduce the need for maximizing sperm production, and so eliminate the pressure to maintain a redundant testis.
  • Female ovaries show no asymmetry in carabid beetles; however, it is expected that the two systems evolved independently, as the male and female gonad primordium probably develop from different parts of the imaginal disc as in Drosophila (Chen and Barker, 1997).

Other Cases of Organ Absence or Extreme Asymmetry

  • For an organ system to completely lack one of a contralateral pair is extremely rare; however, there are a number of notable cases of vestigial and nonfunctional organs, with some groups having an apparently derived loss of one organ.
  • Improved flight is not an issue in Ornithorhynchus , which have two ovaries, but the right one is vestigial and nonfunctional (Grant, 1989).
  • A trend toward reduction of ovariole number in symmetrically paired ovaries and unilateral egg production in non-Scarabaeinae coprophagic beetles is cited as evidence for the repeated occurrence of this phenomenon.
  • In snakes the left lung is reduced but functional in plesiomorphic groups like boids, and vestigial and nonfunctional or absent in more derived groups (Bellairs, 1970; Greene, 1997).
  • These groups do not, however, show absence asymmetry in reproductive organs.

CONCLUSIONS

  • In summary, given the assumption that the internal viscera are subject to adaptive pressure for optimal packing, a testis, redundant and independently developed, is the most likely element to be lost.
  • Other internal organs are not symmetrically paired (fat body), are unitary and/or functionally constrained (tracheae, nerve cord, dorsal vessel, gut, genitalia, muscles, pygidial glands), or probably developmentally and functionally constrained (tracheae, accessory glands).
  • Observations of gross morphology of the male reproductive system and distribution of the monorchid condition allow us to propose this scenario and pressures that could lead to testis loss, but suggest no obvious functional explanation for the reduction of a testis.

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UC Berkeley
UC Berkeley Previously Published Works
Title
Absence Asymmetry: The Evolution of MonorchidBeetles (Insecta: Coleoptera:
Carabidae)
Permalink
https://escholarship.org/uc/item/3pw1g621
Journal
Journal of Morphology, 264(1)
Authors
Will, Kipling
Liebherr, James
Maddison, David
et al.
Publication Date
2005
Peer reviewed
eScholarship.org Powered by the California Digital Library
University of California

Absence Asymmetry: The Evolution of Monorchid
Beetles (Insecta: Coleoptera: Carabidae)
Kipling W. Will,
1
* James K. Liebherr,
2
David R. Maddison,
3
and Jose´ Galia´n
4
1
Department of Environmental Science, Policy and Management, Division of Insect Biology, University of California,
Berkeley, California 94720
2
Department of Entomology, Cornell University, Ithaca, New York 14853-0901
3
Department of Entomology, University of Arizona, Tucson, Arizona 85721
4
Departamento de Biologı´a Animal Facultad de Veterinaria, 30071 Murcia, Spain
ABSTRACT Asymmetrical monorchy, or the complete
absence of one testis coupled with the presence of its
bilateral counterpart, is reported for 174 species of the
carabid beetle tribes Abacetini, Harpalini, and Platynini
(Insecta: Coleoptera: Carabidae) based on a survey of over
820 species from throughout the family. This condition
was not found in examined individuals of any other cara-
bid beetle tribes, or of other adephagan beetle families.
One monorchid taxon within Platynini exhibits symmet-
rical vasa deferentia at the beginning of the pupal sta-
dium, suggesting that developmental arrest of the under-
developed vas deferens takes place in pupation. The point
at which development of the testis is interrupted is un-
known. Complete absence of one organ of a bilateral
pair—absence asymmetry—is rarely found in any animal
clade and among insects is otherwise only known for tes-
tes in the minute-sized beetles of the family Ptiliidae,
ovaries in Scarabaeinae dung beetles, and ovaries of some
aphids. Based on current phylogenetic hypotheses for
Carabidae, testis loss has occurred independently at least
three times, and up to five origins are possible, given the
variation within Abacetini. Clear phylogenetic evidence
for multiple independent origins suggests an adaptive or
functional cause for this asymmetry. A previously posited
taxon-specific hypothesis wherein herbivory in the tribe
Harpalini led to testis loss is rejected. Optimal visceral
packing of the beetle abdomen is suggested as a general
explanation. Specifically, based on the function of various
organ systems, we hypothesize that interaction of internal
organs and pressure to optimize organ size and space
usage in each system led to the multiple origins and main-
tenance of the monorchid condition. Testes are the only
redundant and symmetrically paired structures not
thought to be developmentally linked to other symmetri-
cal structures in the abdomen. Among all possible organs,
they are the most likely—although the observed frequency
is very small—to bypass constraints that maintain bilat-
eral symmetry, resulting in absence asymmetry. However,
based solely on our observations of gross morphology of
internal organs, no function conclusively explains the on-
togenetic loss of one testis in these taxa. Unlike the anal-
ogous absence asymmetry of organs in other animal
groups, no dramatic body-form constraint—e.g., snakes
and lung loss, ptiliid beetles’ small body-size and rela-
tively giant sperm— or adaptive scenario of improved lo-
comotory performance—e.g., birds and ovary loss due to
flight constraints—applies to these carabid beetles. We
tentatively suggest that testis loss is driven wholly by an
interaction among the internal organs of these beetles,
possibly due to selective pressure to maximize the com-
paratively large accessory glands found in these taxa.
However, as the ordering of these evolutionary events of
testis loss and accessory gland size increase is not known,
large accessory glands might have secondarily evolved to
compensate for a decreased testicular output. J. Morphol.
000:000 000, 2005.
© 2005 Wiley-Liss, Inc.
KEY WORDS: ground beetles; absence asymmetry;
monorchy; testis; visceral packing; accessory glands
Asymmetrical loss of a plesiomorphically paired
organ is rare among bilateral metazoan animals.
Among vertebrates, such losses are largely re-
stricted to snakes or snake-like animals, where one
or the other lung has been reduced during evolution
of various lineages (Bellairs, 1970), and to birds,
where most taxa are characterized by the loss of one
ovary (Kinsky, 1971). Monorchy, or the presence of
only one testis, is reported for many nonvertebrate
bilaterian groups. At least some monorchid taxa are
known in the Entoprocta, Gnathostomulida, Nema-
toda, Nematomorpha, Rotifera, Platyhelminthes,
Gastrostichta, Pterobrachia, Tardigrada, Crustacea,
and Chilopoda (Rebecchi et al., 2000; Brusca and
Brusca, 2003). In these taxa, the testis is most likely
either a medial, symmetrical structure resulting
from fusion of paired testes, or an ancestrally bilat-
eral unitary structure.
Among the extremely diverse Insecta, spanning
over a million extant species arrayed across 27 ex-
Contract grant sponsor: National Science Foundation (NSF); Con-
tract grant number: DEB-9981935 (to D.R.M.).
*Correspondence to: Kipling Will, 201 Wellman Hall, ESPM-Insect
Biology, University of California, Berkeley, CA 94720.
E-mail: kiplingw@nature.berkeley.edu
Published online in
Wiley InterScience (www.interscience.wiley.com)
DOI: 10.1002/jmor.10319
JOURNAL OF MORPHOLOGY 000:000 000 (2005)
© 2005 WILEY-LISS, INC.

tant orders, with evolutionary roots in the Devonian
(Gullen and Cranston, 2000; Klass et al., 2002),
there are only four reported instances of the asym-
metrical presence of a primitively paired organ sys-
tem. Three instances are found in the order Co-
leoptera and one in Hemiptera. Two cases are
ovaries that are asymmetrically lost in some scarab
beetles (Halffter and Mathews, 1966; Halffter and
Edmonds, 1982) and in aphids (Woodward et al.,
1970), both taxa wherein females invest extraordi-
narily in relatively few offspring. Feather-winged
beetles (Coleoptera: Ptiliidae) are a third case, char-
acterized by a single testicular mass— based on a
study of eight species representing seven genera
from two subfamilies, Ptiliinae and Acrotrichinae
(de Marzo, 1992). Nossidium pilosellum has paired
vasa deferentia connected to a single, medial testic-
ular mass; the seven other examined species have
the asymmetrical presence of a single testis. Ptiliids
are the smallest known beetles, on average about
0.50 mm, ranging from 0.30–2.0 mm. Additionally,
they are peculiar in having relatively gigantic
sperm, e.g., sperm 1.4 mm long in the 0.7-mm long
beetle Ptinella aptera (Taylor et al., 1982; Dybas and
Dybas, 1987).
The fourth instance is within the usually preda-
ceous beetle family Carabidae (Coleoptera), the sub-
ject of this article. Members of one tribe (Harpalini)
have been previously reported to possess a single
testis on the right side (Dufour, 1825; Smrzˇ, 1981).
We have found asymmetrical monorchy to be more
widespread in carabids than previously reported. In
this article we describe the phylogenetic distribution
of monorchy and discuss its evolution. We show that
monorchy has arisen independently several times
during diversification of taxa comprising the family.
Unlike other reported monorchid conditions in in-
sects or of any other groups, monorchy in Carabidae
has proceeded by the asymmetrical loss of either the
right or left testis. The absence asymmetry of testes
in carabid beetles is therefore a unique type of evo-
lutionary loss among bilateral animals. Whether the
testis is absent due to degeneration of gonad primor-
dia in the embryo or larvae, analogous to mandible
loss in thrips (Heming, 1980, 1993), or whether the
primordial cells never migrate to one side is not
known. Herein we present a comparative study of
carabid testes and suggest that investigation of the
developmental and genetic basis for monorchism in
Carabidae would provide an opportunity to study
the underlying mechanisms that establish bilateral
symmetry in animals and how asymmetries become
unilaterally fixed (Palmer, 1996).
Carabidae
Among the families of the coleopteran suborder
Adephaga, Carabidae, with nearly 40,000 species
(Lorenz, 1998), is the most diverse. Because of the
worldwide geographical distribution of the family
and frequent abundance of individuals of some spe-
cies, more morphological studies have focused on
member taxa than on any other coleopteran family.
Excellent reviews of the history of classification and
phylogenetics (Ball, 1979, 1998), and a comprehen-
sive synopsis noting relationships and distributions
of tribes (Bousquet and Larochelle, 1993) are avail-
able. Recent phylogenetic analyses including exem-
plars from many carabid taxa have focused on a
variety of character systems, e.g., DNA-sequence
data (Maddison et al., 1999; Shull et al., 2001; Ober,
2002), female reproductive tract anatomy (Liebherr
and Will, 1998), larval morphology (Arndt, 1993,
1998; Beutel, 1993), and cuticular and muscular
morphology (Beutel, 1992; Beutel and Haas, 1996).
These studies, given their limitations in taxon sam-
pling and character selection, furnish some insights
into the evolutionary history of the family. All of
these studies agree on several major points; one
presently relevant is monophyly of the subfamily
Harpalinae (sensu Erwin, 1985). Monorchid taxa
presented herein are all members of this subfamilial
clade, thereby sharing a significant number of mor-
phological synapomorphies at that taxonomic level.
Although relationships within Harpalinae are not
understood well enough to allow a mapping of the
evolution of monorchy and diorchy on an explicit
phylogeny, enough is known about the monophyly of
groups that include monorchid taxa to propose min-
imal numbers of origins of the trait.
Given the number of insect species, relatively few
publications present comparative descriptions of the
gross morphology of insect testes and male accessory
glands (Dufour, 1825; Bordas, 1900; Matsuda, 1976;
Suzuki, 1988; Vats and Vasu, 1993; de Marzo, 1992,
1996; Gillott, 2003; Opitz, 2003), although many
publications provide isolated descriptions of male
structures for individual species. Two forms of cole-
opteran testes are known: a single, tubular, coiled
follicle in the suborders Adephaga and Myxophaga
(Reichardt, 1973; Lawrence and Britton, 1994; ques-
tionable in Myxophaga, R. Beutel pers. commun.);
and multiple follicles in the suborders Polyphaga
and Archostemata (Galia´ n and Lawrence, 1993).
Within Polyphaga, follicles may be sessile or pedi-
cellate (Lawrence and Britton, 1994).
Structure of the male testes and accessory glands
has been reported for a significant number of taxa in
Carabidae and a few other adephagan families (Du-
four, 1825; Escherich, 1894, 1898; Bordas, 1900;
Holdhaus, 1913; Jeannel, 1942; Ali, 1967; Smrzˇ,
1981, 1985; Witz, 1990; Yahiro, 1996, Yahiro, 1998;
Carcupino et al., 2002). Even the earliest studies
noted that observed members of Harpalini had no
apparent testis on the left side of the body. Dufour
(1825: 153) interpreted the single testis on the right
side as an agglomeration of two testes, but noted the
presence of only one vesicula seminalis. Bordas
(1900: 310, and plates XIX fig. 6 and XX fig. 1,
wrongly numbered in text, actually plates XVII–
2 K.W. WILL ET AL.

XVIII) claimed that the harpaline taxa he investi-
gated had two equally formed testes. However, both
Smrzˇ (1981) and our study confirm that those taxa
have only one single follicle testis. In all of these
previous studies taxon sampling was limited, re-
gionally circumscribed, and lacked key taxa neces-
sary for understanding the distribution of the con-
dition and its implications for relationships in
Carabidae.
Accessory glands are quite various in insects and
have been studied in many taxa (Chen, 1984; Gillott,
2003). Paired male accessory glands are probably
homologous for all Adephaga. However, gland vari-
ation in position and form across Coleoptera and the
presence of glands in Polyphaga with apparently
distinctly different developmental origins (mesa-
dene and ectadene) (Chapman, 1982) make it diffi-
cult to assess homology at deeper levels.
In this study we comparatively survey testes and
accessory glands across Carabidae. We describe the
gross morphological structure of the reproductive
system and present terminology for several basic
forms of accessory glands. Given the remarkable
asymmetrically monorchid condition in some taxa,
we discuss its implications for understanding bilat-
eral symmetry in animals, establish absence asym-
metry as a subtype of directional asymmetry, and
speculate on causes of its origin and maintenance.
MATERIALS AND METHODS
Specimens were collected and either maintained alive, pre-
served in EtOH (90% or greater), Pampel’s or in Kahle’s fluid
(Barbosa, 1974). Live specimens were anesthetized by placing
them in a freezer at approximately –1°C until completely immo-
bilized. Vivisection was done under distilled water. Ethanol-
preserved specimens were dissected in 95% and other preserved
material under 70% EtOH.
Male reproductive structures were examined in repose in the
abdomen and then excised for further examination. Sketches
were made using a drawing tube mounted on a microscope, then
scanned to create a digital image with drawings completed using
standard image editing software on a personal computer. Alter-
natively, images were taken using a digital camera and drawings
made as an overlay using standard image editing software.
Traditionally, insect specimens preserved in high concentra-
tion EtOH have not been used for morphological study of internal
organs and dried-pinned specimens are generally unsuitable for
studying soft internal tissues. For muscle and organ dissection,
specimens preserved in high-concentration EtOH for later DNA
extraction are inferior to material preserved in FAA or Kahle’s
solutions (compare Fig. 1C,F). Insects are only rarely preserved
in these special fluids, however. Recently, many laboratories and
museums worldwide have begun amassing EtOH-preserved ma-
terial intended for molecular work. This new material contains a
wealth of insect taxa otherwise only known from pinned material.
In order to study very brittle soft-tissue morphological characters
from EtOH material, very slow and careful dissecting technique
is needed and frequent images are taken using a microscope-
mounted digital camera. Essentially, the dissection of a specimen
is documented as layers or structures are removed. Images can
then be directly annotated using image-handling software.
No properly preserved specimens of Amorphomerus were avail-
able, so in this case we determined the state of the testes by
examining a pinned specimen that had been killed in EtOH and
dried. Lateral structures corresponding in position and structure
to testes could be seen in these preparations.
The condition of the early pupal-stage male reproductive tract
was investigated by dissecting pupae that had died following
incomplete molting from the third larval instar. In all such spec-
imens the pupal head was trapped inside its unmolted larval
head capsule. These pupae were preserved in boiling water fol-
lowed by placement in 70% ethanol within 1 day of the attempted
molt. Dissections were made under 70% ethanol, with mercuro-
chrome stain intermittently used to enhance the cuticular struc-
tures.
Emphasis was placed on sampling species and genera within
the monorchid tribes and in groups thought to be closely related
to them. In this study we surveyed or recorded testis condition for
over 820 species. This covers exemplars from all but 14 of the
nearly 80 tribal level groups typically recognized (Bousquet and
Larochelle, 1993). Data derive from several sources: 1) 190 taxa
were examined exclusively for testes; 2) during routine dissec-
tions for two independent chromosome studies, testis condition
was noted for 185 species (Serrano and Galia´n, 1998, their sum-
marized reference numbers 23, 25, 27, 30, 32, and 91), and 167
species (Maddison, 1985); 3) in 185 species testis configurations
were summarized from the other primary literature listed above.
RESULTS
General Description of Male Carabid
Reproductive Tract
Except as noted below, the carabid male reproduc-
tive system is quite typical of insect reproductive
organs. The genital opening lies within the en-
dophallus folded within the median lobe of the ae-
deagus (ml). The ejaculatory duct (ed) emerges from
the foramen of the sclerotized median lobe and ram-
ifies anteriorly into two tubular accessory glands
(ag). These glands vary from relatively small and
simple (Fig. 2C) to large sinuate, convoluted, filling
much of the abdominal cavity and even extending
into the mesothorax (Figs. 1A, 2B). The accessory
glands may be turgid or empty, apparently depen-
dent on breeding condition. We recognize several
conformations of accessory glands. Despite size vari-
ation, their length, shape, and position in the abdo-
men are relatively constant within species.
Our survey of male accessory glands is not as
extensive as that for testes. The four types of acces-
sory glands we recognize here (Fig. 2) are based only
on published illustrations and material dissected by
KWW, and do not include all species known for
testis condition. As noted above, the accessory
glands vary considerably but can be readily recog-
nized as mirror-recurved (Fig. 2A), sinuate (Fig. 2B),
simple (Fig. 2C), or elongate tipped (Fig. 2D). The
simple form (Fig. 2C), which consists of two parame-
dial, tomaculate-form glands, is found in many taxa
including basally divergent carabids (Nebriini) and
much more highly derived (Lebiini, Lachnophorini,
Zuphiini) members of Harpalinae. The elongate tip
form (Fig. 2D) is found only in Rhysodini and Loric-
erini (Smrzˇ, 1981, 1985; Yahiro, 1996; our data). The
tip in Loricera is significantly shorter than that
found in Rhysodini and is likely an independent
derivation of this form. The sinuate form (Fig. 2B) is
the most common and widespread type. Although
variation exists in the number of curves and where
3CARABID BEETLE TESTES

Fig. 1. Internal organs of the male carabid beetle abdomen. Dorsal view with tergites removed. A: Drawing of Selenophorus sp from
Ecuador (Harpalini) showing size and position of male reproductive organs. Other abdomen contents not shown. B: Drawing of
Selenophorus sp from Ecuador showing size and position of internal organs. Digital images of (C) Onypterigia tricolor (Platynini),
preserved in Kahle’s; (D) Platynus brunneomarginatus (Platynini); (E) Amara sp from California (Zabrini); (F) Abacetus (?Caricus)
from Malaysia (Abacetini), preserved in 95% EtOH; (G) Abacetus (Astigis) nitidulus (Abacetini). ag, accessory gland; c, crop; ep,
epididymis; g, gut; pgr, pygidial gland reservoir; ml, median lobe of aedeagus; sc, secretory cells; tVIII, tergite eight; t, testis.
4 K.W. WILL ET AL.

Citations
More filters
Journal ArticleDOI
TL;DR: This review is an attempt to focus attention on this promising but neglected topic by summarizing what the authors know about insect genital asymmetries, and by contrasting this with the situation in spiders, a group in which genitalymmetries are rare.
Abstract: Asymmetries are a pervading phenomenon in otherwise bilaterally symmetric organisms and recent studies have highlighted their potential impact on our understanding of fundamental evolutionary processes like the evolution of development and the selection for morphological novelties caused by behavioural changes. One character system that is particularly promising in this respect is animal genitalia because (1) asymmetries in genitalia have evolved many times convergently, and (2) the taxonomic literature provides a tremendous amount of comparative data on these organs. This review is an attempt to focus attention on this promising but neglected topic by summarizing what we know about insect genital asymmetries, and by contrasting this with the situation in spiders, a group in which genital asymmetries are rare. In spiders, only four independent origins of genital asymmetry are known, two in Theridiidae (Tidarren/ Echinotheridion, Asygyna) and two in Pholcidae (Metagonia, Kaliana). In insects, on the other hand, genital asymmetry is a widespread and common phenomenon. In some insect orders or superorders, genital asymmetry is in the groundplan (e.g. Dictyoptera, Embiidina, Phasmatodea), in others it has evolved multiple times convergently (e.g. Coleoptera, Diptera, Heteroptera, Lepidoptera). Surprisingly, the huge but widely scattered information has not been reviewed for over 70 years. We combine data from studies on taxonomy, mating behaviour, genital mechanics, and phylogeny, to explain why genital asymmetry is so common in insects but so rare in spiders. We identify further fundamental differences between spider and insect genital asymmetries: (1) in most spiders, the direction of asymmetry is random, in most insects it is fixed; (2) in most spiders, asymmetry evolved first (or only) in the female while in insects genital asymmetry is overwhelmingly limited to the male. We thus propose that sexual selection has played a crucial role in the evolution of insect genital asymmetry, via a route that is accessible to insects but not to spiders. The centerpiece in this insect route to asymmetry is changes in mating position. Available evidence strongly suggests that the plesiomorphic neopteran mating position is a female-above position. Changes to male-dominated positions have occurred frequently, and some of the resulting positions require abdominal twisting, flexing, and asymmetric contact between male and female genitalia. Insects with their median unpaired sperm transfer organ may adopt a one-sided asymmetric position and still transfer the whole amount of sperm. Spiders with their paired sperm transfer organs can only mate in symmetrical or alternating two-sided positions without foregoing transfer of half of their sperm. We propose several hypotheses regarding the evolution of genital asymmetry. One explains morphological asymmetry as a mechanical compensation for evolutionary and behavioural changes of mating position. The morphological asymmetry per se is not advantageous, but rather the newly adopted mating position is. The second hypothesis predicts a split of functions between right and left sides. In contrast to the previous hypothesis, morphological asymmetry per se is advantageous. A third hypothesis evokes internal space constraints that favour asymmetric placement and morphology of internal organs and may secondarily affect the genitalia. Further hypotheses appear supported by a few exceptional cases only.

144 citations

Journal ArticleDOI
TL;DR: Structural and behavioral asymmetries in penis' use were examined in detail for a representative species Labidura riparia and revealed that the left penis degenerated in the common ancestor of this group of single‐penis families.
Abstract: The number of penises vary in the insect suborder Forficulina (order Dermaptera; earwigs). Males of the families Diplatyidae, Pigidicranidae, Anisolabididae, Apachyidae, and Labiduridae have two penises (right and left), while those of the Spongipohridae, Chelisochidae, and Forficulidae have a single penis. The proposed phylogenetic relationships among these families suggest that the single-penis families evolved from an ancestor possessing two penises. To date, examinations of double-penis earwig species have found that only a single penis is used per single copulation. These diversities in structural and behavioral aspects of genitalia raises the following intriguing questions: How are the two penises used? Why did a penis degenerate in several earwig families, and which one was lost? To address these questions, structural and behavioral asymmetries were examined in detail for a representative species Labidura riparia (Labiduridae). Although there was no detectable morphological differentiation between the right and left penises, male L. riparia predominantly used the right one for insemination. This significant "right-handedness" developed without any experience of mating and was also manifested in the resting postures of the two penises when not engaged in copulation. However, surgical ablation of the right penis did not influence the insemination capacity of males. In wild-caught males, only about 10% were left-handed; within this group, abnormalities were frequently observed in the right penis. These lines of evidence indicate that the left penis is merely a spare intromittent organ, which most L. riparia males are likely never to use. Additional observations of five species of single-penis families revealed that the left penis degenerated in the common ancestor of this group. Considering the proposed sister relationship between the Labiduridae and the single-penis families, it is possible that such behavioral asymmetries in penis' use, as observed in L. riparia, are parental to the evolutionary degeneration of the infrequently used left penis.

49 citations


Cites background from "Absence asymmetry: the evolution of..."

  • ...Recently, Will et al. (2005) compiled examples and explanations of ‘‘absence asymmetry,’’ i.e., the ‘‘asymmetrical loss of a plesiomorphically paired organ,’’ among animals....

    [...]

  • ...In these cases, the production of large gametes, coupled with space limitations, is a plausible cause for the absence of asymmetry (see Will et al., 2005 for details)....

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Journal ArticleDOI
TL;DR: The morphological characteristics of sperm and reproductive organs may offer clues as to how reproductive systems have evolved, and increased sperm bundle length appears to have been facilitated by the concordance of the sperm bundle’s coiled direction with the coiling direction of the seminal vesicle.
Abstract: The morphological characteristics of sperm and reproductive organs may offer clues as to how reproductive systems have evolved In this paper, the morphologies of the sperm and male reproductive organs of carabid beetles in the tribe Pterostichini (Coleoptera: Carabidae) are described, and the morphological associations among characters are examined All species form sperm bundles in which the head of the sperm was embedded in a rod-shaped structure, ie, spermatodesm The spermatodesm shape (left-handed spiral, right-handed spiral, or without conspicuous spiral structure) and the condition of the sperm on the spermatodesm surface (with the tail free-moving or forming a thin, sheetlike structure) vary among species In all species, the spiral directions of the convoluted seminal vesicles and vasa deferentia are the same on both sides of the body; that is, they show an asymmetric structure The species in which the sperm bundle and the seminal vesicles both have a spiral structure could be classified into two types, with significant differences in sperm-bundle length between the two types The species with a sperm-bundle spiral and seminal-vesicle spiral of almost the same diameter have longer sperm bundles than the species with a sperm-bundle spiral and seminal-vesicle tube of almost the same diameter In the former type, the spiral directions of the sperm bundles and seminal vesicles are inevitably the same, whereas they differ in some species with the later type Therefore, increased sperm bundle length appears to have been facilitated by the concordance of the sperm bundle’s coiling direction with the coiling direction of the seminal vesicle

42 citations


Cites background or result from "Absence asymmetry: the evolution of..."

  • ...Many species in this family have asymmetrically structured reproductive organs (e.g., male genitalia, Yahiro 1998; Will et al. 2005; female genitalia, Liebherr and Will 1998; Bousquet 1999), and thereby, the examination of both the sperm morphology and the reproductive organs in carabids may…...

    [...]

  • ...Many species in this family have asymmetrically structured reproductive organs (e.g., male genitalia, Yahiro 1998; Will et al. 2005; female genitalia, Liebherr and Will 1998; Bousquet 1999), and thereby, the examination of both the sperm morphology and the reproductive organs in carabids may provide insight into the evolution of asymmetric structures in reproductive organs....

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  • ...As reported in previous studies (Liebherr and Will 1998; Bousquet 1999; Will et al. 2005), the sperm storage organ (i....

    [...]

  • ...As reported in previous studies (Liebherr and Will 1998; Bousquet 1999; Will et al. 2005), the sperm storage organ (i.e., spermatheca) of Pterostichini usually has an asymmetric tubular structure....

    [...]

Journal ArticleDOI
19 Jul 2017-PLOS ONE
TL;DR: Using super-resolution microscopy, highly condensed reticulate chromatin is identified in the lancet-shaped spermatozoa heads and the mitochondrial derivates of the flagella, likely formed by genomic and mitochondrial DNA, respectively.
Abstract: Based on advanced light and electron microscopy, we describe the male reproductive system and sperm development of Limodromus assimilis. The genital tract consists of pairs of uni-follicular testes, spermatic ducts with diverticula regions, seminal vesicles, accessory glands, an unpaired ejaculatory duct and an aedeagus containing an internal sac equipped with sclerotic scales. Based on their morphology, we draw conclusions about their functions. After spermatogenesis within the follicle, the spermatozoa become released from the sperm cysts. The single spermatozoa move into the diverticula of the vasa deferentia I. Here, they become attached to central rods (spermatostyles), forming secondary conjugates (spermiozeugmata). The coordinated flagella movement of the conjugates possibly improves sperm velocity. Using super-resolution microscopy, we identified highly condensed reticulate chromatin in the lancet-shaped spermatozoa heads and the mitochondrial derivates of the flagella, likely formed by genomic and mitochondrial DNA, respectively. The results show, for the first time, sperm bundle formation in a Platynini species mainly corresponding to that found in Pterostichini species.

26 citations

References
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MonographDOI
12 Nov 1998
TL;DR: The aim of this monograph is to clarify the role of pheromones and chemicals in the lives of Insects and to propose a strategy to address their role in the food web.
Abstract: The Insects has been the standard textbook in the field since the first edition published over forty years ago. Building on the strengths of Chapman's original text, this long-awaited 5th edition has been revised and expanded by a team of eminent insect physiologists, bringing it fully up-to-date for the molecular era. The chapters retain the successful structure of the earlier editions, focusing on particular functional systems rather than taxonomic groups and making it easy for students to delve into topics without extensive knowledge of taxonomy. The focus is on form and function, bringing together basic anatomy and physiology and examining how these relate to behaviour. This, combined with nearly 600 clear illustrations, provides a comprehensive understanding of how insects work. Now also featuring a richly illustrated prologue by George McGavin, this is an essential text for students, researchers and applied entomologists alike.

2,922 citations

BookDOI
31 Dec 1996
TL;DR: A growing body of evidence has begun to reveal flaws in the traditional assumption of female passivity and lack of discrimination after copulation has begun as discussed by the authors, and evidence from various fields indicates that such selectivity by females may be the norm rather than the exception.
Abstract: A growing body of evidence has begun to reveal flaws in the traditional assumption of female passivity and lack of discrimination after copulation has begun. William Eberhard has compiled an impressive array of research on the ability of females to shape the outcome of mating. He describes studies of many different cryptic mechanisms by which a female can accept a male for copulation but nevertheless reject him as a father. Evidence from various fields indicates that such selectivity by females may be the norm rather than the exception. Because most post-copulatory competition between males for paternity is played out within the bodies of females, female behaviour, morphology, and physiology probably often influence male success in these contests. Eberhard draws examples from a diversity of organisms, ranging from ctenophores to scorpions, nematodes to frogs, and crickets to humans. Cryptic female choice establishes a new bridge between sexual selection theory and reproductive physiology, in particular the physiological effects of male seminal products on female reproductive processes, such as sperm transport, oviposition, and remating. Eberhard interweaves his review of previous s

2,678 citations

Journal ArticleDOI
TL;DR: No new evidence is given as to buffering against environmental stresses of a larger scale, such as temperature or the presence of parasites, but a mean positive correlation between the fluctuating asymmetries of a number of un-
Abstract: Fluctuating asymmetry, discussed below, is commonly used to estimate the effects of minor developmental accidents. These accidents differ between individuals, and there are also individual differences in resistance to these accidents. The ability to resist such developmental accidents will here be referred to as buffering against them. Because of the interrelations of morphogenetic systems, it is possible that an organism well buffered in one character is also well buffered in others, i.e., for this reason the microenvironmental perturbations on different systems in an individual may result in a tendency for the fluctuating asymmetry of different characters in that individual to be higher or lower than usual. Such a correlation in buffering capacities could also-be produced by differences in genotypes and environments acting separately'on different morphogenetic systems, but this is another matter. This investigation concerns the fluctuating asymmetry of different characters. No new evidence is given as to buffering against environmental stresses of a larger scale, such as temperature or the presence of parasites. A mean positive correlation between the fluctuating asymmetries of a number of un-

1,560 citations

Book
01 Dec 1985
TL;DR: This booklet contains useful information on how to select the best book to buy for your home, as well as practical suggestions for improving the quality of the books you buy.
Abstract: *Prices in US$ apply to orders placed in the Americas only. Prices in GBP apply to orders placed in Great Britain only. Prices in € represent the retail prices valid in Germany (unless otherwise indicated). Prices are subject to change without notice. Prices do not include postage and handling if applicable. Free shipping for non-business customers when ordering books at De Gruyter Online. RRP: Recommended Retail Price. Order now! orders@degruyter.com

1,409 citations


"Absence asymmetry: the evolution of..." refers background in this paper

  • ...As the terminalia in carabid beetles are directly involved in copulation, they are presumed to be under strong selective pressure, e.g., mate selection or species isolation mechanisms (Eberhard, 1985, 1996)....

    [...]

  • ...However, reproductive structures in males could be subject to additional pressures such as sperm competition and female-choice (Eberhard, 1985, 1996)....

    [...]

Book
01 Jan 1969

1,235 citations

Frequently Asked Questions (1)
Q1. What are the contributions in "Absence asymmetry: the evolution of monorchidbeetles (insecta: coleoptera: carabidae)" ?

Asymmetrical monorchy, or the complete absence of one testis coupled with the presence of its bilateral counterpart, is reported for 174 species of the carabid beetle tribes Abacetini, Harpalini, and Platynini ( Insecta: Coleoptera: Carabidae ) based on a survey of over 820 species from throughout the family. This condition was not found in examined individuals of any other carabid beetle tribes, or of other adephagan beetle families. One monorchid taxon within Platynini exhibits symmetrical vasa deferentia at the beginning of the pupal stadium, suggesting that developmental arrest of the underdeveloped vas deferens takes place in pupation. Clear phylogenetic evidence for multiple independent origins suggests an adaptive or functional cause for this asymmetry. Optimal visceral packing of the beetle abdomen is suggested as a general explanation. The authors tentatively suggest that testis loss is driven wholly by an interaction among the internal organs of these beetles, possibly due to selective pressure to maximize the comparatively large accessory glands found in these taxa.