Different Asymmetries of the Combative (Sexual) and Cutting (Non-Sexual) Parts of Mandibles in the Horned Stored-Product Beetle Gnatocerus Cornutus (Fabricius, 1798)
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insects Article First Case of Dual Size Asymmetry in an Identical Arthropod Organ: Different Asymmetries of the Combative (Sexual) and Cutting (Non-Sexual) Parts of Mandibles in the Horned Stored-Product Beetle Gnatocerus cornutus (Fabricius, 1798) Tomas Vendl * , Vaclav Stejskal and Radek Aulicky Crop Research Institute, Drnovska 507/73, Prague 6-Ruzyne CZ-16106, Czech Republic; [email protected] (V.S.); [email protected] (R.A.) * Correspondence: [email protected]; Tel.: +420-233-022-360 Received: 24 September 2018; Accepted: 25 October 2018; Published: 29 October 2018 Abstract: Although it is known that separate insect body structures may be asymmetrical within one species, the different functional asymmetries within a single organ as a result of differential selective regimes have not been described. Based on microscopic measurements and SEM photography, we examined the size, shape and asymmetry of the mandibular structures of males and females of the sexually dimorphic broad-horned flour beetle, Gnatocerus cornutus (Tenebrionidae, Coleoptera). It was found that sexual dimorphism only manifests in certain outgrowth parts (horns) of male mandibles, while the remaining cutting parts of the mandibles hold identical morphologies for both sexes. A more interesting finding—since this is the first published case of dual functionally selected asymmetry in an identical arthropod organ—was that the cutting part of the male mandible exhibited directional asymmetry, whereas the outgrowth horn part of the mandible showed a high degree of symmetry. Moreover, there was no relationship between the size and asymmetry of horns. The results indicate different regulatory mechanisms of sexually selected combative horns and the food-functional, more conservative (constrained by hard food and adult long life) cutting parts of mandibles. Keywords: asymmetry; mandibles; secondary sexual trait; sexual dimorphism; stored-product pest 1. Introduction The broad-horned flour beetle, Gnatocerus cornutus, is a tenebrionid stored product pest that is currently on a geographical spread (e.g., it was recently discovered in Japan in 2016 [1]). The species is often found in flour mills, grain warehouses and other facilities [2], and it is morphologically and physiologically adapted to feed on and digest more than 60 various stored agricultural commodities [3]. Not only larvae but also adults are pestilential since they can live and feed upon human resources for up to several months. Apart from the species’ importance in agriculture and the food industry, it is interesting to study from the perspective of behavioral and morphological studies. It is the only synanthropic stored product pest that shows social behavior, and males have fully developed functional combative mandibular horns on their mouthparts (Figure1a,b). Since horns are used as weapons in male–male fights [4], G. cornutus has recently become a model organism in the insect ethology and evolution of sexual traits (e.g., [4–6]). As mentioned above, the G. cornutus adult is a polyphagous and long-lived, and therefore, its mandibles must be functionally adapted not only for fighting (in contrast to, e.g., male stag beetles) but also for physically processing food (e.g., cereals) of Insects 2018, 9, 151; doi:10.3390/insects9040151 www.mdpi.com/journal/insects Insects 2018, 9, 151 2 of 8 Insects 2018, 9, x FOR PEER REVIEW 2 of 8 variedof varied hardiness. hardiness. The The two differenttwo different functional functional roles ofroles one of organ one thusorga potentiallyn thus potentially constitute constitute a striking a interplaystriking interplay and trade-off and trade-off between between selective selective regimes inregimes the development, in the development, size and size symmetry and symmetry of the two of differentthe two different parts of theparts organ. of the organ. FigureFigure 1.1.SEM SEM micrographs micrographs of of the the head head of Gnatocerus of Gnatocerus cornutus cornutus.(a) Dorsal. (a) Dorsal view ofview a male of a head, male ( bhead,) frontal (b) viewfrontal of view a male ofhead, a male (c )head, dorsal (c) view dorsal of view a female of a head. female md: head. mandible; md: mandible; mdh: mandibular mdh: mandibular horn. horn. AlthoughAlthough thethe general general body body plan plan is bilaterallyis bilaterally symmetrical symmetrical in the in majority the majority of animals, of animals, most paired most organspaired manifestorgans manifest more or more less pronouncedor less pronounced degrees degrees of asymmetry. of asymmetry. There can There be asymmetrycan be asymmetry in size asin wellsize as well in shape; as in theshape; latter the being latter a being widespread a widespread phenomenon phenomenon in the animalin the animal kingdom kingdom [7]. The [7]. most The commonmost common form ofform asymmetry of asymmetry is a fluctuating is a fluctuatin asymmetryg asymmetry (FA). FA (FA). is defined FA is as defined a random as deviationa random fromdeviation perfect from symmetry perfect symmetry in paired in traits, paired with traits, no tendencywith no tendency for one for side one to beside larger to be thanlarger the than other the atother the at population the population level level [8–10 [8–10].]. FA originatesFA originates as aas consequence a consequence of of an an individual’s individual’s inability inability to to dealdeal withwith differentdifferent kinds of environmental stresses stresses [8,9]. [8,9]. Directional Directional asymmetry asymmetry (DA) (DA) is isanother another type type of ofasymmetry, asymmetry, which which occurs occurs when when all all individuals individuals have have an an enlarged enlarged left left or or right side. This type ofof asymmetryasymmetry isis usuallyusually adaptive.adaptive. TheThe mandiblesmandibles ofof somesome insectsinsects representrepresent anan exampleexample ofof DA.DA. NotableNotable mandiblemandible DADA isis reportedreported inin snail-feedingsnail-feeding speciesspecies [[11,12],11,12], butbut differentdifferent morphologiesmorphologies ofof thethe leftleft andand rightright mandiblemandible areare commoncommon inin insectsinsects [[13–15].13–15]. Apparently,Apparently, suchsuch asymmetryasymmetry hashas aa functionalfunctional aspect,aspect, asas itit allowsallows thethe mandiblesmandibles toto fitfit intointo eacheach otherother andand thusthus helpshelps toto processprocess food.food. SecondarySecondary sexualsexual traitstraits (i.e.,(i.e., weaponsweapons andand ornaments)ornaments) represent, fromfrom aa symmetrysymmetry perspective,perspective, aa ratherrather special special case. case. It isIt generallyis generally believed believed that sexualthat sexual selection selection favours favours symmetry symmetry [16,17], [16,17], and, indeed, and, excludingindeed, excluding a few exceptions a few exceptions such as chelae such ofas Crustacea chelae of [Crustacea18], sexual [18], traits sexual exhibit traits symmetry exhibit as symmetry a general patternas a general in the pattern majority in the of groupsmajority [19 of]. groups Moreover, [19]. becauseMoreover, sexual because traits sexual are thought traits are to thought be costly to tobe produce,costly to someproduce, studies some suggest studies that suggest their FA that is atheir good FA indicator is a good of male indicator quality of [16male,20 ].quality Nevertheless, [16,20]. aNevertheless, relatively large a relatively amount of large studies amount failed of to studies find a negative failed to relationship find a negative between relationship weapon sizebetween and FAweapon [21–23 size], and and so FA there [21–23], is controversy and so there about is controversy FA as an indicator about FA of males’as an indicator quality. of males’ quality. Horns,Horns, enlargedenlarged mandibles, mandibles, prolonged prolonged forelimbs forelim andbs other and exaggerated other exaggerated structures structures have developed have indeveloped a variety in of a beetle variety lineages of beetle [24 line]. Typically,ages [24]. they Typically, are present they onlyare present in males only [25 ]in and males serve [25] as and weapons serve inas male–maleweapons in combats male–male [26 ].combats Their presence [26]. Their is oftenpresence accompanied is often accompanied by sexual dimorphism by sexual dimorphism in size [27]. Thein size weapons [27]. generallyThe weapons scale positively generally with scale body posi size:tively larger with males body have size: disproportionally larger males largerhave traitsdisproportionally [28], which is larger also the traits case [28], for the which horns is of alsoG. cornutus the case[ 4for]. In the some horns cases, of thereG. cornutus is a developmental [4]. In some thresholdcases, there involved, is a developmental whereby only threshold males above involved a certain, whereby body sizeonly express males theabove trait a [certain28]. body size expressMandibles the trait in[28]. the males of G. cornutus play two functional roles (one in feeding and one in male–maleMandibles combat), in the and males they of are G. thus cornutus presumably play two under functional dual selective roles (one pressure. in feeding During and battles, one in malesmale– usemale de combat), novo developed and they structuresare thus presumably (horns) on theirunder mandibles dual selective [4]. Thepressure. size of During these mandibular battles, males horns use determinesde novo developed the outcome structures of the fight: (horns) the on male their with mand largeribles horns [4]. isThe a better size competitorof these mandibular