Fig 1
Anadenobolus excisus phylogeny summarised from Bond and Sierwald (2002). This phylogeny is based on phylogenetic analyses of ~1030 base pairs of the 16S rRNA mtDNA gene sequenced for 242 individuals (144 unique haplotypes). Each of the three major clades is supported by bootstrap and posterior clade probabilities greater than 98%.
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Jamaican millipedes in the Anadenobolus species complex provide an unusual case study of arthropods having undergone speciation in the absence of conspicuous divergence of male genitalia. Using landmark-based morphometrics, we examined shape deformation of the male anterior copulatory device in three genetically divergent yet morphologically crypti...
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... Anadenobolus excisus species complex comprises three sibling species of Spirobolida millipedes (family Rhinocricidae) that are widely distributed across the Carib- bean island of Jamaica ( Sierwald 2002, 2003). Although morphologically quite similar, these species form exclusive, highly divergent groups based on mitochondrial DNA sequence differences ( Fig. 1 summarised from the phylogeny presented by Bond and Sierwald 2002 based on GenBank Accession nos. AF501371-AF510514). Anadeno- bolus excisus occupies the eastern end of the island, occurring throughout the John Crow Mountains. Anadeno- bolus holomelanus (Pocock) and A. dissimulans Bond and Sierwald occur throughout the central northern and western aspects of Jamaica with narrow sympatric ranges in the central northern areas of their distribution. In this zone of hypothesised secondary contact, populations of A. holo- melanus and A. dissimulans remain genetically cohesive as shown by character displacement in overall body size (Bond and Sierwald 2002). These taxa have thus attained species status under both biological and phylogenetic criteria (Bond and Sierwald 2003). Although millipede species are diag- nosed primarily on the basis of male genitalic differences, our previous qualitative assessments using scanning electron microscopy found no differences among these three species (Bond and Sierwald 2003). Using morphometric techniques, thin plate spline and relative warp analyses, we report studies of genitalic shape that demonstrate subtle, but seemingly incomplete, quantitative shape changes across taxa. This observation, in combination with neutral gene coalescence simulations, suggests that neutral evolution, rather than selection, may best explain patterns of male genital evolution in this ...
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Citations
... Recent studies have demonstrated that speciation may occur without changes in gonopod morphology in several invertebrates (see Bond and Sierwald 2002;Novo et al. 2010). Bond et al. (2003) reported that speciation occurred unaccompanied by gonopod divergence in a spirobolidan millipede, Anadenobolus excisus Karsch, 1881 species complex, and genetic change is uncorrelated to gonopod change. Although intraspecific variation in gonopods is common and differences in gonopod structure among taxa may be subtle (Pimvichai et al. 2011), male gonopods remain the key sources of traits that are used in millipede systematics (cf. ...
... Our results support the position that population divergence and variation in male genitalia of B. flavicollis could be coupled. Bond et al. (2003) concluded based on gonopod morphology that the classification of millipedes may overlook taxonomic diversity due to OTU lumping. Although this might be true in some genera, it does not seem to be the case in B. flavicollis. ...
Male gonopods are useful in taxonomic diagnoses and descriptions of millipedes, although they may vary intraspecifically in shape and size. To assess this intraspecific variation, we used geometric morphometric analysis to compare gonopod morphology among eight isolated populations of the colour-polymorphic southern African millipede Bicoxidens flavicollis . Our results showed that gonopod shapes vary significantly across the examined populations, and elucidated subtle variations. CVA cross-validation test indicates an average classification rate of 75% for the five populations for which we had more than one specimen. Although we had a small number of replicates for three populations, our results still illustrate the importance of applying quantitative approaches to what would otherwise be qualitative and subjective gonopod shape categories in millipedes. As such, the taxonomic assignment of the populations of B. flavicollis may require further investigation, and further revisions would be required with an integrative approach, including molecular data, in order to re-evaluate the taxonomic diversity and distribution data of this species. Finally, we highlight the conservation potential of divergent populations as evolutionary insurance against a dynamic and unpredictable climate, whether or not they undergo full speciation.
... Millipede systematics is mainly based on male gonopods because they use to be species-specific (Bond et al. 2003). However, studies based on DNA have demonstrated that molecular divergence in different millipede groups may not reflect divergence in morphology-based identifications and may hide considerable variation (Bond & Sierwald 2002;Bond et al. 2003;Adams et al. 2009;Mwabvu et al. 2013Mwabvu et al. , 2015Tinago et al. 2017). ...
... Millipede systematics is mainly based on male gonopods because they use to be species-specific (Bond et al. 2003). However, studies based on DNA have demonstrated that molecular divergence in different millipede groups may not reflect divergence in morphology-based identifications and may hide considerable variation (Bond & Sierwald 2002;Bond et al. 2003;Adams et al. 2009;Mwabvu et al. 2013Mwabvu et al. , 2015Tinago et al. 2017). Although our relatively small taxon sampling, the phylogenetic analysis strongly recovers Sechelleptus as monophyletic and discriminates at least two or three different groups. ...
A new millipede species of the genus Sechelleptus Mauriès, 1980 is described and illustrated from Mayotte Island, Indian Ocean. This new species, S. arborivagus sp. nov., found on trees, looks particularly similar to the sympatric S. variabilis VandenSpiegel & Golovatch, 2007, but is much larger and has a very different ecological behavior. Phylogenetic analyses based on a concatenated dataset of the COI and 16S rRNA genes and including nine species of Spirostreptidae (including Sechelleptus, Doratogonus Attems, 1914, Bicoxidens Attems, 1928 and Spirostreptus Brandt, 1833), strongly support the monophyly of Sechelleptus. Despite the similarity of their genitalia, the molecular analyses also reveal a clear-cut genetic divergence between S. arborivagus sp. nov. and S. variabilis (22.55% for COI and 6.63% for 16SrRNA) and further suggest the presence of a higher diversity within the genus Sechelleptus on Mayotte.
... All such species are so similar to one another [Golovatch et al., 2021] that looking for an exact match is more or less useless. The more so as the gonopods in adult ## of Rhinocricidae are long known to grow gradually from one molt to the next and often tend to get modified in the course of hemianamorphosis [Mauriès, 1980;Enghoff et al., 1993;Bond et al., 2003]. ...
... Existing research suggests that body size is more effective in maintaining genetic isolation between sympatric species than genital morphology (Bond and Sierwald, 2002;Tanabe and Sota, 2008). However, it must be kept in mind that many taxonomic works have focused primarily on male genitalia, sometimes to the exclusion of all other morphology (see discussions in Bond et al., 2003;Sierwald et al., 2019). This may be due to the difficulty in observing the invaginated or eversible female genitalia, a perceived lack of divergence in the female genitalia compared to the male genitalia, a cultural bias magnifying the significance placed on male anatomy for sexual selection, or a combination of the above (Ah-King et al., 2014). ...
... In Polydesmus inconstans Latzel, 1883 and Po. complanatus (Linnaeus, 1761) there is a large tubercle extending ventrally from the ventral margin of BR3 (Blower, 1985: fig. 64B; Withrow, 1988: fig. ...
... 61GeL) that are useful for species diagnosis in some taxa. Collectively, these features have been called the epigyne (Blower, 1985). ...
Mate choice, copulation, genital morphology, and sperm storage are not very well understood in millipedes. The use of three-dimensional x-ray computed tomography (μCT) provides new morphological data regarding millipede reproductive systems in both the female and male, including chitinous sclerites and membranes, muscles, glands, oviducts, and sperm conduits. Here we present a complete integrated account of the morphology and function of the female genital organs in the family Polydesmidae (Diplopoda: Polydesmida) using μCT, UV fluorescence imaging, and scanning electron microscopy. These data allow us to consider competing hypotheses regarding millipede vulva formation. We additionally present the morphology of copulatory interface in Pseudopolydesmus Attems, 1898 using images of a mating pair in copula and by simulating the interface of the organs using 3D models from μCT, allowing us to tentatively identify a lock-and-key-like mechanism. Finally, we use μCT to reveal the topology of the seminal canal in the gonopod of male Pseudopolydesmus, a topic that has remained unresolved for nearly 80 years.
... The cryptic nature of SS hinders investigation, making comparisons of SS and lock-and-key challenging. However, a small number of authors have undertaken this task and found evidence for lock-and-key or neutral/pleiotropic evolution of gonopod shape (Wojcieszek & Simmons, 2012;Bond et al., 2003;Tanabe & Sota, 2008). The research is ongoing, and further studies are needed before a general understanding of the drivers of genitalic variation can develop, especially if multiple mechanisms could be at play. ...
... 38). The genitalic differences provide a straightforward basis for naming new species (but see the tautology discussed by Bond et al., 2003). Though useful for species-level alpha-taxonomy, pronounced morphological differences between closely related species mask synapomorphies among higher-level taxa. ...
For the past several centuries, millipede taxonomists have used the morphology of male copulatory structures (modified legs called gonopods), which are strongly variable and suggestive of species-level differences, as a source to understand taxon relationships. Millipedes in the family Xystodesmidae are blind, dispersal-limited and have narrow habitat requirements. Therefore, geographical proximity may instead be a better predictor of evolutionary relationship than morphology, especially since gonopodal anatomy is extremely divergent and similarities may be masked by evolutionary convergence. Here we provide a phylogenetics-based test of the power of morphological versus geographical character sets for resolving phylogenetic relationships in xystodesmid millipedes. Molecular data from 90 species-group taxa in the family were included in a six-gene phylogenetic analysis to provide the basis for comparing trees generated from these alternative character sets. The molecular phylogeny was compared to topologies representing three hypotheses: (1) a prior classification formulated using morphological and geographical data, (2) hierarchical groupings derived from Euclidean geographical distance, and (3) one based solely on morphological data. Euclidean geographical distance was not found to be a better predictor of evolutionary relationship than the prior classification, the latter of which was the most similar to the molecular topology. However, all three of the alternative topologies were highly divergent (Bayes factor >10) from the molecular topology, with the tree inferred exclusively from morphology being the most divergent. The results of this analysis show that a high degree of morphological convergence from substantial gonopod shape divergence generated spurious phylogenetic relationships. These results indicate the impact that a high degree of morphological homoplasy may have had on prior treatments of the family. Using the results of our phylogenetic analysis, we make several changes to the classification of the family, including transferring the rare state-threatened species Sigmoria whiteheadi Shelley, 1986 to the genus Apheloria Chamberlin, 1921—a relationship not readily apparent based on morphology alone. We show that while gonopod differences are a premier source of taxonomic characters to diagnose species pairwise, the traits should be viewed critically as taxonomic features uniting higher levels.
... Numerous studies have found that millipede genital structures evolve rapidly and divergently resulting in species specific variation, which allow species recognition (Hosken and Stockley 2004;Eberhard 2010). However, there is a more recent body of evidence which demonstrates that male genital divergence may proceed at a slower rate than genetic divergence and speciation may occur without any change in gonopod morphology (Bond et al. 2003;Adams et al. 2009;Wojcieszek and Simmons 2012). If there is a lack of conspicuous differences in male genital structures between recently divergent species, then morphologically cryptic species will have evolved. ...
... This study demonstrates that the presence of divergent mitochondrial lineages is not unique to B. flavicollis alone but is also apparent in B. brincki and B. friendi. For taxa such as millipedes, the presence of divergent mitochondrial lineages despite the absence of discrete variation in gonopod morphology often suggests the presence of hidden diversity (Bond and Sierwald 2002;Bond et al. 2003). Furthermore, the present study indicates the existence of four distinct mitochondrial lineages within B. flavicollis populations, which is previously unreported. ...
Two recent studies have suggested that divergent mitochondrial lineages may be present within spirostreptid genera such as Bicoxidens Attems, 1928. Bicoxidens, similar to many other endemic soil invertebrates, exhibits low dispersal capabilities and strict microclimate habitat preferences, attributes that often lead to geographic isolation. Given that prolonged geographic isolation often lays the foundation for population genetic differentiation, genetic divergence and possibly speciation, there was good reason to suspect that Bicoxidens may consist of several distinct lineages. On this basis, the mitochondrial cytochrome c oxidase subunit 1 (COI) was used to reconstruct the phylogeny of Bicoxidens and reveal divergent lineages within the genus. Maximum likelihood and Bayesian inference analyses recovered a paraphyletic Bicoxidens phylogram with divergent lineages present in three species – B. friendi, B. flavicollis and B. brincki – suggesting high genetic diversity within the genus. Bayesian genetic cluster analyses suggested the presence of multiple distinct mitochondrial lineages within the genus with four identified in B. flavicollis alone. It was therefore concluded that the divergent lineages observed among Bicoxidens populations may suggest the presence of hidden species.
... Although male genitalia are central in spirostreptid millipede taxonomy (see Hoffman 2008;Hamer 2009;Mwabvu et al. 2010) because they are divergent and species specific (Bond et al. 2003), morphology-based classifications may be too inclusive (Adams et al. 2009;Ács et al. 2010) and may hide considerable variation. Molecular data have demon strated in many arthropod groups that molecular divergence may not reflect divergence in morphology, thus resulting in an underestimation of diversity (Brewer et al. 2012). ...
... Derkarabetian et al. (2011) also reported a lack of divergence in reproductive morphology in Opiliones, although genetic divergence is significant. Other studies, for example, in Anadenobolus millipedes (Bond et al. 2003) and spiders (Huber et al. 2005), also suggest that genetic and genitalic divergence are decoupled. Hence, groups that were described on the basis of morphological characters are being re-evaluated using appropriately variable DNA sequence data. ...
The aim of this study was to use cytochrome c oxidase 1 (CO1) sequences to recover a phylogeny for seven morphologically described spirostreptid millipede taxa from southern Africa, and to evaluate the correspondence between morphological and molecular phylogenies. Genetic p-distance generally increased with taxonomic divergence: inter-specific mean 15.33 % (14.09 % –17.02 %), inter-generic mean 18.43 % (6.83 %–26.81 %) and inter-order mean 24.16 % (range 18.56 %–30.77 %). Congruent Bayesian, maximum parsimony and neighbour-joining analyses of 520 nucleotides of the CO1 gene resolved the orders Spirostreptida, Julida and Callipodida. Members of genera within the Spirostreptidae (Archispirostreptus, Bicoxidens, Cacuminostreptus, Doratogonus, Orthoporoides, Plagiotaphrus and Spirostreptus) formed a single clade within which a sample of Thyropygus (family Harpagophoridae) was paraphyletically nested. Phylogenetic analyses failed to recover support for the genera Doratogonus, Bicoxidens, Archispirostreptus and Spirostreptus, as representatives of these genera were not monophyletic. Samples morphologically identified as the same species (Bicoxidens flavicollis) were part of two different clades, one of which was well supported and otherwise contained members of Doratogonus. This high level of divergence (mean 12.64 %) between morphologically identified spirostreptid millipede sister species could indicate that changes in genital morphology occur rather slowly relative to CO1 sequence substitution, and may underestimate species diversity.
... Studies suggest that strong directional sexual selection (both pre-and postcopulatory) acting on these traits can lead to rapid differentiation, and that these structures could be subject to continuous change (Birkhead & Pizzari, 2002;Gavrilets, 2000;McPeek, Shen, Torrey, & Farid, 2008;Panhuis et al., 2001). However, it is likely that these male traits are often subject to frequent episodes of directional selection interspersed with periods of stabilizing selection within isolated populations (Bond, Beamer, Hedin, & Sierwald, 2003;Simmons, House, Hunt, & Garcia-Gonzalez, 2009;Wojcieszek & Simmons, 2012). In A. diversiformis, I found strong between-male variation in most femur and genital shape traits but moderate to no systematic differentiation between Costa Rican and Panamanian populations (Figs. 3 and 4). ...
Reproductive traits often evolve rapidly, and some suggest that behavioural traits, in particular, can diverge faster than morphology, resulting in sexual isolation between populations/species. An earlier study of a Neotropical dung fly, Archisepsis diversiformis (Diptera: Sepsidae), reported anecdotally that two central American populations that were approximately 500 km apart (Costa Rica and Panama) differed in male courtship behaviour despite being morphologically similar. Here, I present results of an in-depth study designed (1) to test whether these two populations show qualitative and/or quantitative differences in mating behaviour and morphology, (2) to test whether individuals from either population show some degree of reproductive isolation and (3) to characterize population variation in a particularly fast evolving mitochondrial gene fragment, cytochrome oxidase c subunit I (COI), to estimate genetic differences between the two populations. Despite similarities in overall courtship, I identified behaviours that were clearly population specific, and report that both populations showed strong premating isolation in one-on-one crosses. However, after extended exposure in mass-container group crosses, individuals did produce adult F1 offspring, suggesting that isolation is incomplete. Surprisingly, morphometric analyses indicated that these two populations differed significantly in sexually mono- morphic adult wing shape but differed only moderately in sexually dimorphic male forefemur shape, and not at all in male genital clasper shape. Finally, both populations were genetically similar, forming a single, monophyletic cluster with low uncorrected pairwise distances (COI threshold <1 %), suggesting that marked behavioural differences between both populations have evolved quickly but without complete isolation.
... Lombardo 2000; Battiston & Fontana 2005;Jensen et al. 2009;) and other arthropod groups (e.g. Bond et al. 2003;Polihronakis 2009). Finally, morphological divergence in A. aptera and A. bolivari was also supported by all the studied traits related with body size (Table 1). ...
The genus Apteromantis Werner, 1931 comprises two species of wingless mantids, the Iberian A. aptera (Fuente, 1894) and the North African A. bolivari (Werner, 1929). Although A. aptera and A. bolivari have been traditionally considered as separate and valid species, their external appearance is quite similar and no comprehensive taxonomic study has analyzed their morphological and genetic characteristics. This taxonomic uncertainty has important implications for conservation because A. aptera is considered an Iberian endemic and the only praying mantis protected by international laws. In this study, we apply a comprehensive approach, including quantitative morphological and molecular analyses, to shed new light on the taxonomic and conservation status of the genus Apteromantis and the putative species. We have found that the Iberian and North African specimens analyzed herein significantly differ in female head shape, male genitalia morphology and several other traits related to body size. Molecular data suggest the presence of two main lineages, with sequence divergence rates of approximately 4 %, which are within the range reported for other well defined insect species. Overall, this study supports that A. aptera and A. bolivari are valid species despite their ecological and morphological similarity and highlights the importance of comprehensive approaches to resolve old taxonomic and conservation problems.
... Lombardo 2000; Battiston & Fontana 2005;Jensen et al. 2009;) and other arthropod groups (e.g. Bond et al. 2003;Polihronakis 2009). Finally, morphological divergence in A. aptera and A. bolivari was also supported by all the studied traits related with body size (Table 1). ...
Apteromantis aptera is a rare mantis with discontinuous distribution and the reduction of Mediterranean habitats may threaten it in the future; however, at the present time it is widespread in the Iberian peninsula and this grants a good resistance to this threat. In recent years, since the last assessment, its presence has been recorded in many new localities, almost doubling its EOO. Now it is not only a Spanish endemic but its presence is also well known in Portugal. Complete data on distribution, the main population trends and ecology are still scarce or absent but the quality of information has been locally improved in recent years, giving a good general point of view on this species. Due to these changes in the knowledge base for this species it is felt that the category for this species should be downgraded from Vulnerable to Least Concern.
