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Non-Commercial Use Only Journal Journal of Entomological of Entomological and Acarologicaland Acarological Research Research 2017; 2012; volume volume 49:6680 44:e ENTOMOLOGY The insect antenna: segmentation, patterning and positional homology A. Minelli Department of Biology, University of Padova, Italy temporal pattern of division along the flagellum depends on local Abstract cues, or on signals travelling along the whole proximo-distal axis of the appendage. The basic mechanism by which the antennal flagellum is sub- divided into flagellomeres is probably the same in all insects, irre- spective of whether the process occurs in the embryo, in the eye/antenna imaginal disc, or through a series of post-embryonic Introduction increments punctuated by moults. The ultimate origin of (all?) fla- gellomeres is the first antennomere following the pedicel, from Three distinct processes are relevant to an assessment of posi- which split off in apical direction new primary flagellomeres, each tional homology between specific features, or markers, restricted of which is eventually the source of secondary flagellomeres, to one or more antennomeresonly of an insect antenna (Figure 1): i) the according to specific spatial and temporal patterns subject to het- primary proximo-distal patterning into scape, pedicel and flagel- erochrony. Only a detailed knowledge of the underlying segmen- lum; ii) the segmentation of the flagellum into flagellomeres; iii) tation processes could provide the ultimate background for deter- the regional patterning of the flagellum, producing specializations mining positional homology between flagellomeres of two anten- such as lateraluse projections, sensory structures or an apical club nae with different number of antennomeres. The antennae of the involving a restricted number of flagellomeres. Heteroptera are likely re-segmented, as their second antennomere The articulation of the antenna into scape, pedicel and flagellum seems to include a flagellar component. The larval antennae of the is nearly universally conserved (but see below); therefore, this level holometabolans are temporal serial homologues of those of the of proximo-distal patterning is generally unproblematic in respect to adult, but their segmental composition is problematic. Significant the assessment of homology between specific antennomeres of two progress will be done by understanding what differentiates anten- insects. To the contrary, the process by which the flagellum is seg- nomeres that divide, either embryonically or post-embryonically, mented, and its timing in respect to the patterning of the flagellom- from those that do not; and by discovering whether the spatial and eres, is relevant to the assessment of positional homology. This point is best illustrated with reference to an insect group in which the total number of antennomeres is largely but not universally fixed, as are the Coleoptera, most of which have antennae of 11 Correspondence: Alessandro Minelli, Department of Biology, antennomeres. The extensive conservation of this number suggests University of Padova, via Ugo Bassi 58B, 35131 Padova, Italy. that we can suppose an equally conserved segmentation process, E-mail: [email protected] thus a conservation of the relative positional value of the individual Key words: Heterochrony; Meriston; Pentatomidae; Positional homolo- antennomeres. Under such circumstances, the fifth antennomere, gy; Resegmentation. for example, can be regarded as the same in all beetles with anten- Non-commercialnae of 11 antennomeres. Things are different when antennae with Acknowledgements: the author is grateful to Giuseppe Fusco and to an different number of antennomeres are compared. For example, how anonymous referee for their critical comments on a draft version of this to trace homologies between the individual antennomeres of a 9- article. antennomere beetle antenna and those of an antenna with the usual Conflict of interest: the author declares no potential conflict of interest. 11 antennomeres (Figure 1)? To answer the question we should know the sequence of events by which the flagellum acquires seg- Received for publication: 2 March 2017. mentation. Unfortunately, current knowledge about this process is Revision received: 10 April 2017. very poor for the holometabolous insects, from both the morpholog- Accepted for publication: 10 April 2017. ical and genetic points of view. A f ©Copyright A. Minelli, 2017 irst difficulty to be addressed is the fact that the segmenta- Licensee PAGEPress, Italy tion of the insect antenna occurs under different and not obviously Journal of Entomological and Acarological Research 2017; 49:6680 comparable conditions. Important sequences of segmentation hap- doi:10.4081/jear.2017.6680 pen during formative stages, that is, either in the embryo or in the pupa, but in most non-holometabolous insects there is also a more This article is distributed under the terms of the Creative Commons overt phase of increase in the number of antennomeres during the Attribution Noncommercial License (by-nc 4.0) which permits any noncommercial use, distribution, and reproduction in any medium, post-embryonic development. Differences between embryonic or provided the original author(s) and source are credited. pupal antennal segmentation and postembryonic addition of antennomeres are not limited to the much easier access to the latter [Journal of Entomological and Acarological Research 2017; 49:6680] [page 59] Article than to the former, but are also exacerbated by the widespread divides a variable number of times, thus giving off a series of off- although implicit assumption that the post-embryonic segmenta- spring articles that are progressively pushed towards the distal end tion of the antenna is fundamentally different from the embryonic of the antenna. In most non-holometabolous insects, the divisions or pupal one – whatever fundamental may eventually mean. of the meriston are binary, but in the Mantophasmatodea the meris- In this article, I suggest that the process of segmentation of the ton divides five times into three flagellomeres at each time insect antenna (of its flagellum in particular) is to some extent the (Hockman et al., 2009). same irrespective of the time it occurs, in the framework of the ani- The subsequent fate of the articles split off from the meriston is mal’s embryonic or post-embryonic development, except perhaps diverse. In some insect groups, these articles do not split anymore. for the larval antenna of the holometabolans. Interpreting the dif- For example, in the whole post-embryonic development of the ferences in the segmentation of the antenna of all insects essential- Zoraptera there is only a binary division of the meriston with the ly as temporal (heterochronic) variations of one basic developmen- moult from the second to the third instar (the total number of anten- tal theme will suggest i) a new framework for tracing homologies nomeres growing this way from 8 to 9) and no further division of between antennomeres that is likely applicable to all insects (and antennal articles will follow (Mashimo et al., 2014); similarly, none possibly also to other arthropods, malacostracan crustaceans espe- of the flagellomeres split off the meriston of the Mantophasmatodea cially) and ii) a targeted research agenda on the mechanisms of undergoes subsequent splitting (Hockman et al., 2009). In other antennal segmentation. insects, the flagellomeres that split off from the meriston undergo further, but limited, splitting, often following stereotyped sequences, with some difference from group to group. For example, divisions of flagellomeres at various positions along the flagellum are observed, Segmentation of the antenna in non-holometabolous e.g., in the Blattodea (Schafer, 1973) and the Orthoptera. The insects sequence of post-embryonic segmentation of the locust Dociostaurus maroccanus (Thunberg, 1815) reconstructed by Paoli In the majority of non-holometabolous insects, the process of (1937) and reproduced as exemplary for hemimetabolans in Imms’s segmentation of the antenna is partly embryonic, partly post- (1940) classic paper on growth processes in the antennae of insects, embryonic. In other terms, the number of antennomeres generally is reproduced here (Figure 2), and interpreted in the light of the increases also throughout the series of post-embryonic moults. The hypothesis presented in this onlyarticle. final number of antennomeres is fixed in some orders, variable in Insects, those with the longest antennae included, are arguably others, often with some degree of intraspecific variation, especially not the best arthropod group where to look for a model in which to in antennae with dozen of flagellomeres. study of the segmentation of the flagellum. Terminal flagella The main source of new antennomeres is always the most (Boxshall, 2004;use 2013) are present, indeed, also in appendages of proximal flagellomere, or meriston (Henson, 1947). This segment other taxa, for example in both the first and the second antennae of Non-commercial Figure 2, Segmentation of the antenna in Dociostaurus maroc- canus, based on Paoli (1937) (part of the sequence to the right of the vertical line) and extrapolated into the embryonic phase of Figure 1. Positional homology between individual antennomeres development (left of the vertical line) according to the model dis- of two insects is unambiguous when the total number of anten- cussed in the text. Post-embryonic splits of flagellomeres are nomeres is the same (a, homology;
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