Fig 1.
Phylogenetic timeline and citation chart.
On the top: phylogenetic timeline illustrating history of phylogenetic studies in dung beetles. Description of the phylogenetic studies is provided in Table 1. Left on the bottom: citation chart of Coleoptera subfamilies. The popularity of each Coleoptera subfamily is based on the number of citations on Google Scholar. The diagram shows the 16 most popular Coleoptera subfamilies whose number of citations exceed 1500. The citations were obtained by querying a recently updated list of all Coleoptera subfamilies (provided by Alfred Newton, Field Museum, Chicago, IL) in Google Scholar using R script (available upon request). Scarabaeinae emerges as the second top subfamily, with 4740 citations. Numbers above columns indicate the number of citations.
Table 1.
The key phylogenetic studies in the subfamily Scarabaeinae.
See also phylogenetic time-line in Fig. 1.
Fig 2.
Phylogenetic patterns revealed by previous phylogenies.
The trees illustrate relationships, among tribes Onthophagini, Oniticellini, Onitini, Sisyphini, Eurysternini, Deltochilini and some genera. Interrupted line indicates remote relationship between clades i.e., it omits irrelevant taxa/clades branching between the clades it joins.
Table 2.
Abbreviations used in the text.
Table 3.
Description of parameter-partition schemes tested using Bayesian framework.
Fig 3.
Ontology of Scarabaeinae and partitioning schemes used in Bayesian analyses.
a, Graph of Scarabaeinae ontology reflecting anatomical characters relationship from datamatrix. This graph guided generation of partitioning schemes in Bayesian analyses. The tips of the graph refer to elementary categories of characters and their relative size correspond to the number of characters in the category. The abbreviations and uniquely colored pictures of beetle anatomical part associated with each tip specify the elementary category (see Table 4.) b-d, exemplified partitioning schemes: the uniquely colored tips of the graph above beetle picture characterize partitions used in Bayesian analyses; abbreviations (see Table 4) associated with tips specify the elementary categories included in the partition; the beetle body parts are colored in accordance with the partition they belong to. The number # indicates the ID of partitioning scheme from Table 5. e, The remainder partitioning schemes demonstrated without graphs. Beetle body parts are colored in accordance with the partition they belong to. The number # indicates the ID of partitioning scheme from Table 5.
Table 4.
Elementary categories and associated characters.
Table 5.
Partitioning schemes.
Fig 4.
Strict consensus of parsimonious trees of Scarabaeinae, with Bremer support values.
a, Strict consensus tree with Bremer support values from the analysis #1; unweighted parsimony, dataset with all characters. b, Strict consensus tree with Bremer support values from the analysis #5; unweighted parsimony, dataset excluding characters #122, 71, 73, 74, 161, 204.
Fig 5.
Majority consensus of parsimonious trees of Scarabaeinae.
a, Majority consensus (50%) of MPTs from the analysis #1; unweighted parsimony, dataset with all characters. b, Majority consensus (50%) of MPTs from the analysis #5; unweighted parsimony, dataset excluding characters #122, 71, 73, 74, 161, 204.
Table 6.
Summary of statistics for parsimony phylogenetic analyses.
Fig 6.
Phylogenetic tree of Scarabaeinae from parsimony analysis #5 (implied weight parsimony, dataset excluding characters #122, 71, 73, 74, 161, 204), with mapped synapomorphies.
This topology was obtained with concavity factor ranging from 40 to 100. In addition to this tree, this range of factors also yielded two other MPTs. Those two parsimonious trees differs only in the position of the clade (Hammondantus psammophilus + Pycnopanelus krikkeni) which is highlighted in orange and its alternative positions are arrowed. Branches of the tree are colored according to the Scarabaeinae taxonomy.
Fig 7.
Phylogenetic tree of Scarabaeinae from parsimony analysis #5 with implied weights (same tree as in Fig. 6, see that figure for description).
Branches of the tree are colored according to the area of endemism of the genus. The scheme of biogeographic regions is provided on the top of the figure (note: the Palearctic and Oriental Regions are combined for clarity). The photographs of beetles correspond to the taxa used in the analyses.
Fig 8.
Comparison of model likelihoods.
#ID of model correspond to the specific parameter-partition scheme described in Table 3 and S3 Table. The red and blue columns, on the plot, corresponding to dataset with and without autapomorphies respectively, show variation of likelihood values (max and min) from different runs within specific parameter-partition scheme. a, comparison of model likelihoods estimated using harmonic mean method. b, comparison of model likelihoods estimated using stepping stone and harmonic mean methods.
Fig 9.
Summary of trees from Bayesian analyses.
Top figures, 4 phylogenetic trees with removed tip labels from the Bayesian analyses corresponding to the best partition-parameter model (complete tree can be found in S5–S7 Figs.). The branches colored in red on trees #9.3 and #8.11 show clades unique to those trees in comparison to the tree corresponding to the model #6.9 (without autapomorphic characters) that has highest model likelihood among all the analyses. The branches colored in red on #6.9 show unique clades in comparison to #9.3 (without autapomorphic characters). Model #6.9 and #8.11 have the highest average model likelihood in the analyses with unlinked rate multiplier, while model #9.3 is the best in analyses with linked rate multiplier. The trees corresponding to the models are placed in color boxes indicating inclusion or exclusion autapomorphies. Beetle figures and associated descriptions under the tree illustrate parameter-partition schemes used in the analyses. The large central tree was obtained from the scheme, with the highest model likelihood, #6.9 (without autapomorphic characters). Clade values correspond to posterior probabilities. The clade Q, which recovered only in Bayesian analyses, is highlighted.
Fig 10.
Genitalic elements of Scarabaeinae.
a-g, Odontoloma sp.; h, Sarophorus costatus; i-l, Byrrhidium namaquensis; m-n, Dicranocara deschodti; o-q, Nebulasilvius insularis; a-d, h, i, aedeagal sac with sclerites; e, l, aedeagus, lateral view; f, aedeagus, dorsal view; g, aedeagus, ventral view; j-k, m-n, o-p, aedeagal sclerites; q, scheme of intact aedeagal sclerites.
Fig 11.
Genitalic elements of Scarabaeinae.
b-d, Paraphytus sp.; g-h, Coptorhina auspicata; e-f, Frankenbergerius armatus; a-c, aedeagal sclerites; g, e, scheme of intact aedeagal sclerites; h, f, scheme of dissected aedeagal sclerites; d, phallobase, dorsal view.
Fig 12.
Genitalic elements of Scarabaeinae.
a-b, Delopleurus sp.; c-d, Bohepilissus sp.; e-f, Anachalcos convexus; g-i, Epirinus sp.; a, d, f, scheme of intact aedeagal sclerites; b, scheme of dissected aedeagal sclerites; e, SRP sclerite; g, i, picture scheme of aedeagal sclerites; h, aedeagus, dorsal view; i, phallobase, left lateral view.
Fig 13.
Genitalic elements of Scarabaeinae.
a-c, Amphistomus calcaratus; d,e, Tanzanolus sp.; f, Agamopus lampros; g, Anomiopus edmondsi; h, Agamopus viridis; i, Aphengium cupreum; a, f-i, picture scheme of aedeagal sclerites; b, aedeagus, dorsal view; c, aedeagus, lateral left view; d, e, aedeagal sac with sclerites.
Fig 14.
Genitalic elements of Scarabaeinae.
a, Ateuchus squalidus; b, Aphengoecus multiserratus; c, Aulacopris maximus; d, e, Bdelyropsis bowditchi; f-h Bdelyrus seminudus; a-d, h, picture scheme of aedeagal sclerites; e, g, aedeagus, lateral left view; f, aedeagus, dorsal view.
Fig 15.
Aedeagus of Onthophagus avocetta.
b-d, Onthophagus avocetta; e,f, Bubas bison; g, h, i, Helictopleurus quadripunctatus; a, position of aedeagus at rest inside abdomen, dorsal view; b, aedeagus with aedeagal sclerites, ventral-lateral oblique view. Note: pictures of aedeagi in blue circles are used in figures of this paper to show the relative position of aedeagus to illustrated sclerite(s). In this figure the aedeagi in blue circles are located at the tips of respective imaginary axes indicating the direction of view; the text associated with the circles indicate the terms used for describing aedeagus position and directions. c-g, i, scheme of intact aedeagal sclerites; h, lamella copulatrix.
Fig 16.
Genitalic elements of Scarabaeinae.
a, Gen. nov. sp. nov.; b, Boletoscapter cornutus; c, Deltochilum sp.; d, Canthidium bokermanni; a-d, picture scheme of aedeagal sclerites.
Fig 17.
Genitalic elements of Scarabaeinae.
a-d Canthochilum tureyra; e-f, Canthonella silphoides; g, Canthon virens; h-j, Canthonosoma macleayi; k-m, Catharsius sp.; n, Circellium bacchus; a, aedeagus, frontal view; b, aedeagus, right lateral view; c-d, g-h, m, n, picture scheme of aedeagal sclerites; e, i, k, aedeagus dorsal view; f, j, l, aedeagus left lateral view.
Fig 18.
Genitalic elements of Scarabaeinae.
a, Chalcocopris hesperus; b, Cephalodesmius armiger; c, Coproecus hemisphaericus; d, Copris sp.; e, Copris; f, Coprophanaeus telamon; a-c, f, picture scheme of aedeagal sclerites; d, picture scheme of aedeagal sclerites, sclerites disarticulated; e, scheme of intact aedeagal sclerites.
Fig 19.
Genitalic elements of Scarabaeinae.
a, Coptodactyla nitida; b-d, Cryptocanthon paradoxus; e Demarziella interrupta; f, Dichotomius sericeus; g, Dichotomius sp; a, d-f, picture scheme of aedeagal sclerites; b, aedeagus dorsal view; c, aedeagus left lateral view; g, lamella copulatrix.
Fig 20.
Genitalic elements of Scarabaeinae.
a, Diorygopyx tibialis; b-c, h, Ennearabdus lobocephalus; d-f, Epactoides sp1.; g, Epactoides sp2.; i-k, Eurysternus hamaticollis; a, d, g, h, k, picture scheme of aedeagal sclerites; b, e, j, aedeagus dorsal view; c, f, i, aedeagus left lateral view.
Fig 21.
Genitalic elements of Scarabaeinae.
a, Eucranium arachnoides; b-c, Genieridium margareteae; d-f, Dwesasilvasedis medinae; g, Glyphoderus monticola; a,-c, f, g, picture scheme of aedeagal sclerites; d, aedeagus dorsal view; e, aedeagus left lateral view.
Fig 22.
Genitalic elements of Scarabaeinae.
a-b, Gromphas aeruginosa; c-e, Gymnopleurus leei; f, Gyronotus carinatus; g-i, Hammondantus psammophilus; a, c, f, i, picture scheme of aedeagal sclerites; b, d, aedeagus dorsal view; e, h, aedeagus left lateral view; g, aedeagus right lateral view.
Fig 23.
Genitalic elements of Scarabaeinae.
a, Hansreia sp.; b, Homocopris torulosus; c, Heliocopris sp.; d, Janssensantus pauliani; e, Macroderes mutilans; f-h, Ochicanthon sp.; a-e, h, picture scheme of aedeagal sclerites; f, aedeagus dorsal view; g, h, aedeagus left lateral view.
Fig 24.
Genitalic elements of Scarabaeinae.
a-c, Arachnodes sp.; d, Mentophilus hollandiae; e, Megathoposoma candezei; f-g, Malagoniella yucateca; a, d, e, g, picture scheme of aedeagal sclerites; b, f, aedeagus right lateral view; c, aedeagus dorsal view.
Fig 25.
Genitalic elements of Scarabaeinae.
a, Metacatharsius sp.; b, Microcopris sp.; c, Onitis; d, Onitis sp.; e, Onoreidium howdeni; f, Onthobium gutierrezi; a, b, d-f, picture scheme of aedeagal sclerites; c, scheme of aedeagal sclerites.
Fig 26.
Genitalic elements of Scarabaeinae.
a-c, Ontherus appendiculatus; d, Oruscatus davus; e, Scarabaeus aesculapius; f, Paragymnopleurus sp.; g, Pedaria sp.; a, d, e, f, g, picture scheme of aedeagal sclerites; b, aedeagus dorsal view. b, aedeagus left lateral view.
Fig 27.
Genitalic elements of Scarabaeinae.
a, b, Paracanthon sp.; c, Pseudonthobium sinuatotibiale; d, Phanaeus splendidulus; a-d, picture scheme of aedeagal sclerites.
Fig 28.
Genitalic elements of Scarabaeinae.
a, Pseudopedaria grossa; b-e, Pycnopanelus krikkeni; f, Saphobius sp.; g-i, Scarabaeus aegyptiorum; a, e, g, f, picture scheme of aedeagal sclerites; b, h, aedeagus, right lateral view; c, aedeagus, phallobase, dorsal view; d, aedeagus, left lateral view; i, aedeagus, dorsal view.
Fig 29.
Genitalic elements of Scarabaeinae.
a, Scatimus strandi; b, Scatonomus fasciculatus; c-e, Scybalocanthon nigriceps; f, Scybalophagus rugosus; g, Sylvicanthon bridarollii; a-c, f, g, picture scheme of aedeagal sclerites; d, aedeagus, dorsal view; e, aedeagus, left lateral view.
Fig 30.
Genitalic elements of Scarabaeinae.
a-c, Sinapisoma sp.; d-f, Streblopus opatroides; g, Tesserodon erratum; h, Neosisyphus sp.; a, d, g, h, picture scheme of aedeagal sclerites; b, e, aedeagus, dorsal view; c, f, aedeagus, left lateral view.
Fig 31.
Genitalic elements of Scarabaeinae.
a, Tetraechma sanguineomaculata; b, Uroxys epipleuralis; c, Uroxys latesulcatus; d, Uroxys pauliani; a-d, picture scheme of aedeagal sclerites.
Fig 32.
Genitalic elements of Scarabaeinae.
a, Xinidium dentilabris; b-c, Zonocopris gibbicollis; d-i, Trichillum pauliani; a, b, d, picture scheme of aedeagal sclerites; c, aedeagus right lateral view; f, aedeagus dorsal view; c, aedeagus left lateral view; g, intact aedeagal sac with sclerites; h, i, scheme of aedeagal sclerites.
Fig 33.
Genitalic elements of Scarabaeinae.
a, b, Aphodius erraticus; c, d, Endroedyolus paradoxus; e, Epirinus sp.; f, Podotenus fulviventris; g, Xinidium dentilabris; h, Macroderes mutilans; i, Dicranocara deschodti; j, Demarziella interrupta; l, Tesserodoniella elguetai; k, Ateuchus histeroides; a, d, aedeagus dorsal view; b, aedeagus ventral view; c, g, h, aedeagus lateral view; e, aedeagus rear view; f, spiculum gastrale, lateral view; i, j, spiculum gastrale; k. l, picture scheme of aedeagal sclerites.
Fig 34.
a, Odontoloma sp.; b, Endroedyolus paradoxus; c, Dicranocara deschodti; d, Byrrhidium namaquensis; e, Frankenbergerius armatus; f, Delopleurus sp.; g, Sarophorus costatus; h, Paraphytus sp.; i, Epirinus sp.; j, Neosisyphus sp.; k, Janssensantus pauliani; l, Aphengoecus multiserratus; m, Pycnopanelus krikkeni; n, Bohepilissus sp.; o, Macroderes mutilans; p, Xinidium dentilabris; q, Pedaria sp.; r, Gyronotus carinatus; a-r, right elytron, lateral view. Elytral striae are enumerated; indistinct striae or their traces are marked by *.
Fig 35.
a, Dwesasilvasedis medinae; b, Anachalcos convexus; c, Coptodactyla nitida; d, Amphistomus calcaratus; e, Boletoscapter cornutus; f, Demarziella interrupta; g, Diorygopyx tibialis; h, Onthobium gutierrezi; i, Bdelyrus seminudus; j, Bdelyropsis bowditchi; k, Tesserodoniella elguetai; l, Canthochilum tureyra; m, Canthonella silphoides; n, Cryptocanthon paradoxus; o, Paracanthon sp.; p, Streblopus opatroides; q, Zonocopris gibbicollis; r, Genieridium margareteae; a-r, right elytron, lateral view. Elytral striae are enumerated; indistinct striae or their traces are marked by *.
Fig 36.
a, Aphengium cupreum; b, Ateuchus sp1.; c, Ateuchus sp2.; d, Scatimus strandi; e, Canthidium bokermanni; f, Uroxys epipleuralis; g, Uroxys pauliani; h, Homocopris torulosus; i, Ontherus appendiculatus; j, Uroxys latesulcatus; k, Canthon virens; l, Hansreia sp.; m, Anomiopus edmondsi; n, Megathoposoma candezei; o, Sinapisoma sp.; p, Copris sp.; q, Catharsius sp.; r, Metacatharsius sp.; a-r, right elytron, lateral view. Elytral striae are enumerated; indistinct striae or their traces are marked by *.
Fig 37.
a, Eucranium arachnoides; b, Ennearabdus lobocephalus; c, Gromphas aeruginosa; d, Oruscatus davus; e, Ochicanthon sp.; f, Arachnodes sp.; g, Scarabaeus sp.; h, Eurysternus hamaticollis; i, Tanzanolus sp.; a-i, right elytron, lateral view. Elytral striae are enumerated; indistinct striae or their traces are marked by *.
Fig 38.
a, Neosisyphus sp.; b, Sarophorus costatus; c, Pycnopanelus krikkeni; d, Pedaria sp.; e, Hammondantus psammophilus; f, Frankenbergerius armatus; g, Epirinus sp.; h, Delopleurus sp.; i, Coptorhina auspicata; a-i, wings. Wing venation annotated in Fig. 41a, b.
Fig 39.
a, Coptodactyla nitida; b, Ochicanthon sp.; c, Metacatharsius sp.; d, Dichotomius sericeus; e, Megathoposoma candezei; f, Canthon virens; g, Gymnopleurus leei; h, Canthidium bokermanni; i, Gromphas aeruginosa; j, Ontherus sulcator; a-j, wings. Wing venation annotated in Fig. 41a, b.
Fig 40.
a, Xinidium dentilabris; b, Sinapisoma sp.; c, Scatimus strandi; d, Oruscatus davus; e, Zonocopris gibbicollis; f, Eurysternus hamaticollis; g, Bdelyrus seminudus; h, Homocopris torulosus; i, Onthophagus sp.; j, Onthophagus sp.; k, Trichillum pauliani; a-h, wings. Wing venation annotated in Fig. 41a, b.
Fig 41.
Wings and gula of Scarabaeinae.
a, Copris sp.; b, Onitis sp.; c, Podotenus fulviventris; d, Xinidium dentilabris; e, Sarophorus costatus; a-c, wings; d,e, gula dorsal view.
Fig 42.
a, e, g, Macroderes mutilans; b-d, h, Byrrhidium namaquensis; f, Delopleurus sp.; a-b, mentum-glossae, dorsal view; c, epipharynx, dorsal view; d-f, left mandible, ventral view; g-h, mandibles, ventral view.
Fig 43.
a,b,e, Chalcocopris hesperus; c,f, Glyphoderus monticola; d, Scatonomus fasciculatus; g,h, Eucranium arachnoides; i,j, Ateuchus squalidus; k, Megathoposoma candezei; a,c,i, hypopharynx and glossae, dorsal view, left maxillary palpus removed; b, hypopharynx and glossae, left lateral view; d,h, left maxilla, ventral view; e, epipharynx, ventral view; f, epipharynx, dorsal view; g, molar lobe of right mandible; j, hypopharynx and glossae, fronto-dorsal view, left maxillary palpus removed; k, hypopharynx and glossa, frontal view, both maxillary palpus removed, left glossa also removed.
Fig 44.
a,e,n, Scarabaeus aesculapius; b, Anachalcos convexus; c, Streblopus opatroides; d,f, Chalcocopris hesperus; h, Heliocopris sp; i, Copris sp.; j, Coptodactyla nitida; k, Zonocopris gibbicollis; l, Metacatharsius sp.; m, Eurysternus hamaticollis; a,c, hypopharynx and glossae, dorsal view, left maxillary palpus removed; b, hypopharynx and glossae, left lateral view, left maxillary palpus removed; d, left maxilla ventral view, stipital sclerite II; f, left maxilla dorsal view, dorsal articular sclerite of galea arrowed; g,h, right maxilla, dorsal view, sclerite of lacinia removed, basal sclerite of galea arrowed; i-k, epipharynx, ventral view; l, hypopharynx and glossae, dorsal view, both maxillary palpus removed; m, hypopharynx and glossae, right lateral view. n, right mandible, left lateral view.
Fig 45.
Morphological structures of Scarabaeinae.
a, Aulacopris maximus; b, Dichotomius sericeus; c, Onthophagus seniculus; d, Aphengium sordidum Harold, 1868; e, Zonocopris gibbicollis; f, Cryptocanthon paradoxus; g, Anomiopus edmondsi; h, Eurysternus hamaticollis; i, Neosisyphus sp.; j, Sarophorus costatus; k, Coptodactyla nitida; l, Hansreia sp.; m, Epactoides sp1.; n, Pseudonthobium sinuatotibiale; a, head ventral view; b, head left lateral view; c, antennal club; d, clypeus ventral view; e, head frontal view; f, head dorsal view; g, h, k, l, m, prothorax, ventral view; i, prothorax, dorsal view; j, prothorax, ventral view, propleurae and prosternum removed; n, fore tarsi, bifurcation of claws arrowed.
Fig 46.
Morphological structures of Scarabaeinae.
a, Coptodactyla glabricollis; b, Boletoscapter cornutus; c, Bdelyropsis bowditchi; d, Pseudonthobium sinuatotibiale; e, Paragymnopleurus sp.; f, Coptorhina auspicata; g, Ochicanthon sp.; h, Bdelyropsis bowditchi; i, Trichillum pauliani; j, Paraphytus sp.; k, Podotenus fulviventris; l, Pachysoma aesculapius; m, Agamopus viridis; a, femur and trochanter of foreleg; b, apical portion of fore tibia, lamella-like setae arrowed; c, pygidium; d, fore tarsus; e, f, pterothorax, lateral view; g, abdomen, lateral view, sternites enumerated; h-l, abdomen ventral view, sternites partly enumerated; m, internal structure of pterothorax, dorsal view.
Fig 47.
Morphological structures of Scarabaeinae.
a, Zonocopris gibbicollis; b, Onthophagus vinctus Erichson, 1843; c, Endroedyolus paradoxus; d, Gymnopleurus leei; e, Aphengium cupreum; f, Coprophanaeus telamon; g, Zonocopris gibbicollis; h, Onthophagus muticifrons Endrödi, 1973 a, pterothorax, ventral view; b, abdomen, ventral view; c, pygidium; d, abdomen, dorsal view; e, apex of metepisternum, lateral view; f, metanotum; g, mesotarsus; h, pterothorax, lateral view.