While comparative studies on antennal sensilla morphology in insects are rare (Hallberg and Hansson 1999), we attempt here to relate the comparative morphology of antennal sensilla, as a proxy for the evolutionary impact of underlying chemical communication, with species diversity and diversification rates. General morphology of antennal sensilla is rather uniform in most insects, mainly composed of sensilla trichodea (e.g., Hallberg and Hansson 1999, Nowińska and Brożek 2017; Yuvaraj et al. 2018); this could be one cause for the lack of overarching studies in beetles and other insect groups. This, however, is not the case in scarabaeiform beetles in which at least 44 different sensilla types have been reported so far (Meinecke 1975; Scholtz 1990; Bohacz et al. 2020).
The general patterns of antennal sensilla morphology reported here suggest that there is an apparent link between the evolution of placoid sensilla and the association with angiosperms (including phytophagous feeding) (Fig. 3). This trend is possibly even parallel, as many taxa in the Liparetrinae + Aclopinae, sister to the remainder Pleurosticti have mostly sensilla trichodea (Fig. 3; Suppl. Figures 6, 8; Bohacz et al. 2020), while ancestral state of the latter remains uncertain yet since in all ancestral lineages already prevail placoid sensilla, either round or elongate ones.
No direct relation between species diversity or rate of diversification and general sensilla morphology was found, instead. This could be explained by the fact that some lineages with placoid sensilla include only few species belonging often phylogenetically isolated rogue lineages of uncertain systematic placement (e.g., Phaenomeridinae, Euchirini, Pachypodini), which were addressed in this study too. Many more were not yet included or just poorly sampled due to either insufficient available specimens (e.g., the polyphyletic Tanyproctini; Eberle et al. 2019) or the lack of DNA data for certain lineages, thus being not represented yet in the available molecular phylogenies (Hunt et al. 2007; Bocak et al. 2014; Ahrens et al. 2014; Timmermanns et al. 2016; Zhang et al. 2018; Song and Zhang 2018; McKenna et al. 2019; Neito Moreno et al. 2019; Ayivi et al. 2021; Cai et al. 2021). Moreover, there are also several lineages with exclusively trichoid sensilla that are quite diverse such as scarab dung beetles (Scarabaeinae, Aphodiinae) or stag beetles (Lucanidae) (Table 1).
We refrained here from a sister group comparison (e.g., Slowinski and Guyer 1993) due to two reasons: 1) existence of only one clear major shift from sensilla trichodea to placoid-like sensilla at the root of the clade (Melolonthinae + Rutelinae + Cetoniinae + Dynastinae) Pleurostict chafers (green dot, Fig. 3), while 2) the shift among Liparetrinae and Aclopinae is rather patchily known yet and in the known cases often quite gradual which requires a much denser lineage sampling for being able to link the sensilla morphology with exact number of species diversity or the rate of evolution. Yet, Pleurostict chafers, particularly the clade (Melolonthinae + Rutelinae + Cetoniinae + Dynastinae), are the most diverse lineage of Scarabaeoidea. Thus, the connection of chemical communication/ sensilla morphology (i.e., a tendency to placoid sensilla) and diversification success continues being needed to be explored further in detail, particularly also because Zhang et al. (2018) reported, in comparison to all other scarabaeiform beetles, significantly increased diversification rates for Scarabaeidae, which in their tree included dung beetle lineages (Scarabaeinae + Aphodiinae) and phytophagous Pleurosticts.
We expect that chemical communication is rather more complex than it would become apparent from the simple examination of sensilla morphology. Sensilla trichodea prevail also in all hyperdiverse phytophagous beetle lineages of Phytophaga with no increased antennal surface (e.g., Ritcey and McIver 1990; Ranger et al. 2017; Vera and Bergmann 2018; Di Palma et al. 2019; Dong et al. 2020), thus high performance in chemical sensing is not necessarily linked with complicated or highly modified sensilla structure (e.g., Symonds et al. 2011). For instance, Rutelinae and Melolonthinae, although having in many lineages quite similar placoid sensilla, differ completely in their pheromone compounds (Melolonthinae: amino acid derivatives and terpenoids; Rutelinae: fatty acid derivatives; Leal 1998). Since "Melolonthinae" referred in Leal (1998) to unrelated lineages of Liparetrini, Rhizotrogini and Melolonthini, it is uncertain, whether these compounds could be part of an "ancestral" phylogenetical pattern or if they do represent lineage specific components. Chapman (1982) suggested that insects with a generalist diet require a greater number of sensilla than species with a more specialized diet, a hypothesis which is, however, only moderately supported by more recent studies (Lopez et al. 2014).
Last but not least, the high plasticity of sensillar morphology, which was already noticed by Meinecke (1975) based on histological analyses, makes the extraction of categorical data and discrete character states difficult in a comparative context. However, such plasticity is less common in the much less diverse early lineages of Scarabaeoidea (besides prominent exceptions such as in Glaresidae, Bolboceratidae, Glaphyridae, or Ochodaeidae; Fig. 3). This might be a starting point for further hypotheses to test, particularly when exploring sensilla variation in the context of pheromone diversity which is so far rather fragmentarily known.
Interestingly, placoid sensilla (although with much inferior morphological diversity) are also known in other, less diverse beetle lineages with antenna that have an increased antennomere surface (Ramsey et al. 2015). However, increased antennomere surface is not generally linked to the presence of placoid sensilla, as e.g., in Drilidae with pectinate antenna yet only sensilla trichodea occur (Faucheux and Kundrata 2017). Nevertheless, Ramsey et al. (2015) argue that the elaborate lamellate antennae, such as in male Rhipicera beetles, increases the surface area, which changes the airflow across the antennae, and thus the likelihood of odorant-receptor interactions (Jaffar-Bandjee et al. 2020). The latter is supposed to have an impact, in consequence, to the sensilla morphology and their efficacy.