Research Article |
Corresponding author: Georgina Rodriguez ( georginarodriguez87@gmail.com ) Academic editor: Martin Fikácek
© 2022 Miguel Archangelsky, Georgina Rodriguez, Patricia Laura María Torres.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Archangelsky M, Rodriguez G, Torres PLM (2022) Testing the monophyly of Chaetarthriinae (Coleoptera, Hydrophilidae) and the phylogenetic position of Guyanobius with larval characters. Arthropod Systematics & Phylogeny 80: 229-242. https://doi.org/10.3897/asp.80.e76826
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The subfamily Chaetarthriinae includes morphologically distinct larvae that are adapted to a diversity of environments. Based on larval characters, cladistic analyses (maximum parsimony (MP) and Bayesian inference (BI) with homoplasy as a partitioning scheme) were performed to test the monophyly of the subfamily and the relationships of the two tribes included in it: Chaetarthriini and Anacaenini. The chaetotaxy of a third instar larva Guyanobius adocetus is described and illustrated in detail, including morphometric characters. This larva is compared to those of the known larvae of the tribe Chaetarthriini belonging to the genus Chaetarthria, and Pseudorygmodus, Crenitis, and Crenitulus from Anacaenini. None of the unconstrained analyses recover Chaetarthriinae as monophyletic. Chaetarthria diverges in an early branch, probably due to a series of unique morphological modifications associated with a riparian lifestyle whereas Guyanobius appears closely related to Anacaenini. Two alternative positions of Guyanobius are revealed: (1) as sister of all Anacaenini (unconstrained MP) or (2) nested within Anacaenini as sister of Crenitis + Crenitulus (constrained MP and unconstrained BI). The genera Paracymus and Tormus (tribe Laccobiini) diverge as two successive branches subordinate to Chaetarthriinae (excluding Chaetarthria) in the unconstrained MP analysis. However, the support is rather weak, and the position of Paracymus and Tormus is an artifact produced by some homoplastic characters. In this regard, homoplasy partitioning resulted a useful technique to solve some artifacts generated by convergent morphologies.
Hydrophiloidea, larvae, morphology, phylogeny, homoplasy, adaptive convergence, parsimony, Bayesian inference, water scavenger beetles.
The Chaetarthriinae are a small group of morphological unique water scavenger beetles. This subfamily was erected by
The genus Guyanobius Spangler, 1986 belongs to the tribe Chaetarthriini (
Guyanobius, which includes the larger members within the tribe, comprises four neotropical species restricted to northern South America. The genus was erected by
Larvae of Guyanobius adocetus have been described by
Although relationships among Chaetarthriinae have been assessed with molecular data (
One third-instar larva of G. adocetus was studied. Guyana, Mazaruni-Potaro district, Takutu Mountains, 6°15’ N, 59°5’ W, 3–10.xii.1983, P. J. Spangler, R.A. Faitoute and P.D. Perkins leg.
For comparative purposes, larvae of Chaetarthria bruchi and unidentified larvae of Chaetarthria from Montana (USA) were examined. Information on C. seminulum comes from the literature (
Larval specimens were cleared in warm lactic acid, dissected, and mounted on glass slides with Hoyer’s medium. Observations (up to 1.000 ×), photographs and drawings were made with a Leica S6D dissecting microscope and a Leica DMLB compound microscope, both with a camera lucida and a photographic camera attached.
Different measurements of the head capsule and head appendages were taken with a micrometer. Measurements were used to calculate ratios, which are useful for characterizing shapes. Measured structures were adjusted as parallel as possible to the plane of the objective. The following measurements were taken. TL: total body length; MW: maximum body width, measured at level of prothorax; HL: head length, measured medially along epicranial stem from anterior margin of frontoclypeus to occipital foramen; HW: maximum head width; AL: length of antenna, derived by adding the lengths of the first (A1L), second (A2L) and third (A3L) antennomeres; SeL: length of antennal sensorium; SL: length of stipes; MPL: length of maxillary palpus, obtained by adding the lengths of the first (MP1L), second (MP2L), third (MP3L) and fourth (MP4L) palpomeres; ML: length of maxilla, derived by adding SL and MPL, cardo omitted; LPL: length of labial palpus, obtained by adding the lengths of the first (LP1L) and second (LP2L) palpomeres; LigL: length of ligula; MtW: maximum width of mentum; PrmtL: length of prementum, measured from its base to the base of LP1; PrmtW: maximum width of prementum.
Primary (present in first-instar larva) and secondary (arising in later instars) setae and pores were identified in the cephalic capsule and head appendages. Since only a third instar larva was studied, the primary chaetotaxy was interpreted and coded by comparison with Chaetarthria larvae and also with other hydrophilid genera for which the chaetotaxy is well known (e.g., Enochrus, Hydramara, Tropisternus, etc.) (
For the analysis 27 taxa, belonging to 14 tribes of Hydrophilidae were included; Helophorus liguricus Angus 1970 (Helophoridae) was used as the outgroup to root the trees (Supplementary file 1). The resulting matrix had 128 larval characters (Supplementary file 2). The data matrix was built with Mesquite (Maddison & Maddison, 2019), and analyzed with TNT (
Since larvae of Paracymus-group appeared nested within Chaetarthriinae in our analyses and considering that based on molecular evidence they are not closely related, we performed a second analysis forcing the monophyly of Chaetarthriinae to examine the effect of Tormus + Paracymus on the topology. The analysis was implemented with the TNT define constraints option, and the constrained searches were carried out using the unconstrained settings.
In addition, we performed a Bayesian inference (BI) analysis using homoplasy as a partitioning criterion of discrete morphological characters (see
The following combination of characters distinguishes Guyanobius larvae from any other known hydrophilid larvae.
Head capsule subquadrate (Fig.
Frons with six secondary setae on each side along inner margin of frontal lines; gFR1 with eight setae, six stout, dorsal setae and two smaller setae ventrally, below two dorsal innermost setae; gFR2 with four stout setae, bifid apically; FR1 short and stout; pores FR15 not closely aggregated. Parietale with setae PA13 and PA14 closely aggregated; seta PA16 short; PA26–28 forming a triangle. Antenna with AN9 absent; SE1 as long as A3. Mandible with MN1 rather long, on basal fifth; minute seta MN5 closer to pore MN4 than to apex; MN2–4 forming a triangle. Maxilla with seta MX7 slender; setae MX8–11 stout and bifid apically; two secondary setae on ventral side near seta MX5; seta MX24 very long. Labium with 18 secondary setae on mentum along outer and anterolateral corners; seta LA5 rather long; seta LA10 at base of ligula; pore LA11 sub-basal. Morphometric measures are detailed in Table
Measurements (in mm) and ratios for different structures of third instar larva of G. adocetus. Abbreviations: see Material and Methods section.
Measure | G. adocetus L3 | Measure | G. adocetus L3 |
TL | 5.02 | SL/MPL | 1.00 |
MW | 0.89 | MP1L | 0.04 |
HL | 0.32 | MP2L | 0.03 |
HW | 0.51 | MP3L | 0.03 |
HL/HW | 0.63 | MP4L | 0.04 |
AL | 0.20 | ML | 0.28 |
A1 | 0,08 | LPL | 0.04 |
A2 | 0.08 | LP1L | 0.01 |
A3 | 0.04 | LP2L | 0.03 |
SeL | 0.04 | LP2L/LP1L | 3.00 |
SeL/A3 | 1.00 | LigL | 0.07 |
A1/A2 | 1.00 | LigL/LPL | 1.75 |
A1/(A2+A3) | 0.67 | MtW | 0.11 |
HL/AL | 1.60 | PrmtW | 0.06 |
HW/AL | 2.55 | PrmtL | 0.04 |
SL | 0.14 | PrmtW/PrmtL | 1.50 |
MPL | 0.14 | PrmtW/MtW | 0.55 |
Head capsule
(Figs
The unconstrained MP analysis produced one most parsimonious tree (549 steps); the tree with support values is shown in Fig.
Figure
To test if the resultant topology of the unconstrained analysis was not affected by the inclusion of Paracymus + Tormus, we performed a constrained MP forcing Chaetarthriinae monophyly. This analysis generated two most parsimonious trees (554 steps) with no differences in the divergence patterns for the subfamily; a detail of the Chaetarthriinae clade is shown in Figure
The unconstrained BI with homoplasy as a partitioning scheme does not recover neither the subfamily nor the tribes as monophyletic (Fig.
Larval knowledge of Chaetarthriini is rather limited, of the six recognized genera (four if Apurebium and Venezuelobium are considered variants of Chaetarthria) only Chaetarthria and Guyanobius have known larvae. Within Guyanobius, only the larva of G. adocetus has been described; therefore, within the tribe it can only be compared with larvae of Chaetarthria.
Comparative table of morphological and chaetotaxic characters among known Chaetarthriinae larvae (third instars). Anacaena is not included since its chaetotaxy has not been described.
Chaetarthriini | Anacaenini | ||||
Character | Chaetarthria | Guyanobius | Crenitis | Crenitulus | Pseudorygmodus |
Nasale, symmetry | symmetrical | symmetrical | asymmetrical | asymmetrical | asymmetrical |
Nasale, teeth | 3 teeth, middle one much longer | 5 teeth | 5 teeth | 5 teeth | 5 teeth, lateral ones grouped |
Epistomal lobes with inner spines | present | present | absent | absent | absent |
Frontal lines | subparallel, widely separated basally | lyriform, converging towards base of head capsule | lyriform, converging towards base of head capsule | lyriform, converging towards base of head capsule | lyriform, converging towards base of head capsule |
Stemmata | closely aggregated, difficult to count | 6 distinctly separated | 6 distinctly separated | 6 distinctly separated | 6 distinctly separated |
Antennal sculpture | A1 and A2 smooth | A1 and A2 with sharp cuticular spines | A1 and A2 with sharp cuticular spines | A1 and A2 with sharp cuticular spines | A1 and A2 smooth |
Antenna | A1 not wider than A2, A3 as long as wide | A1 distinctly wider than A2, A3 longer than wide | A1 distinctly wider than A2, A3 longer than wide | A1 distinctly wider than A2, A3 longer than wide | A1 slightly wider than A2, A3 longer than wide |
Mandible | with 2 retinacula | with 3 retinacula | with 3 retinacula | with 3 retinacula | with 2 retinacula |
Stipes | without spine | with a stout apical spine on inner margin | without spine | without spine | without spine |
Maxillary palpomere 1 | smooth | with sharp dorsal and mesal cuticular spines | with sharp dorsal and mesal cuticular spines | with sharp dorsal and mesal cuticular spines | with sharp dorsal and mesal cuticular spines |
Maxillary palpomere 1 | incompletely sclerotized | incompletely sclerotized | completely sclerotized | incompletely sclerotized | incompletely sclerotized |
Mentum | as wide as prementum | much wider than prementum | much wider than prementum | much wider than prementum | much wider than prementum |
Prementum | incompletely sclerotized dorsally | completely sclerotized | completely sclerotized | completely sclerotized | completely sclerotized |
Ligula | round, as long as labial palpi | elongate, subtriangular, longer than labial palpi | elongate, subtriangular, longer than labial palpi | elongate, subtriangular, longer than labial palpi | elongate, subtriangular, longer than labial palpi |
Pronotal plate | without lateral projections | without lateral projections | with lateral projections | with lateral projections | with lateral projections |
Legs | reduced, 3-segmented | normal, 5-segmented | normal, 5-segmented | normal, 5-segmented | normal, 5-segmented |
Thoracic and abdominal pleura | slightly lobed | strongly lobed | strongly lobed | slightly lobed | strongly lobed |
Abdominal tergum VIII | divided | entire | entire | entire | entire |
Posterior margin of tergum VIII | not trifurcated | not trifurcated | trifurcated | trifurcated | trifurcated |
Head capsule, latero-ventrally with many secondary setae | absent | absent | present | present | absent |
gFR1 | with 6 setae | with 8 setae | with 6 setae | with 6 setae | with 8 setae |
gFR2 | 3–4 simple setae | 4 bifid apically setae | 4 simple setae | 4 simple setae | 3 simple setae |
Secondary setae along frontal lines | at most 5 setae | at least 8 stout setae | 3–4 setae | 1 seta | no secondary setae |
Setae FR4-6 | arranged in a triangle | arranged in a straight line | arranged in a straight line | arranged in a triangle | arranged in a triangle |
Seta FR12 position | posterior to FR13 | posterior to FR13 | anterior to FR13 | anterior to FR13 | anterior to FR13 |
Pore PA6 position | distant from frontal lines | distant from frontal lines | close to frontal lines | close to frontal lines | close to frontal lines |
Setae MX8-11 | apex simple | bifid apically | apex simple | apex simple | apex simple |
Seta MX21 position | closer to inner edge of palpomere | closer to inner edge of palpomere | closer to inner edge of palpomere | closer to outer edge of palpomere | closer to outer edge of palpomere |
Seta LA3 | very long, slender | short, stout | short, slender | long, slender | ? |
Pore LA8 position | distal | at midlength | distal | distal | distal |
Seta LA10 position | on intersegmental membrane | at base of ligula | on intersegmental membrane | on intersegmental membrane | ? |
Pore LA11 position on ligula | at midlength | basal | at midlength | at midlength | ? |
Chaetarthriinae was raised to subfamily level quite recently (
Neither the monophyly of Chaetarthriinae nor that of its tribes is supported by larval characters. Our results are in contrast to those analyses based on molecular data (
The unusual morphology of Chaetarthria places it in a basal position, diverging early from the other taxa. This was expected since these larvae are unique within Hydrophilidae and display a high degree of modifications to the labroclypeus, stemmata, labium and legs, all of which are most likely related to a riparian lifestyle. For instance, these larvae present three unique apomorphies (Fig.
The convergent larval morphology of Paracymus and Tormus with Chaetarthriinae (excluding Chaetarthria) also causes many problems in reconstructing the phylogeny of the group. Until quite recently, Paracymus was considered part of Anacaenini based on adult morphology (
Paracymus larvae share several character states in common with Chaetarthriinae larvae. However, all of these characters are highly homoplastic and no unique synapomorphy can be mentioned. All of these features are shared with several genera of the family Hydrophilidae such as character 9(1) asymmetric nasale; characters 23(3) and 24(3) right and left mandibles with 3 retinacular teeth; character 61(1) pore FR2 inserted equidistant from FR1 and FR3; character 80(1) short sensilla PA20, character 92(2) pore MX3 in line with MX4 on the stipes; among others. In the case of Tormus, in addition to several homoplastic synapomorphies, there is a unique feature that supports the grouping with Chaetarthriinae (except Chaetarthria): character 19(1) surface of A1 with groups of fine cuticular spicules. Although not present in this work, this character state was also reported for Enigmahydrus and Saphydrus (Hydrophilidae: Cylominae) (see
In spite of having two alternative positions within the Chaetarthriinae, all analyses agree that Guyanobius appears to be more closely related to Anacaenini than to Chaetarthriini. This clade is supported by nine homoplastic synapomorphies in the unconstrained MP analysis (Fig.
The clade Pseudorygmodus + Crenitis + Crenitulus (Fig.
This paper provides a first insight into the relationships among the Chaetarthriinae based on larval morphological characters. The results of our work are affected by the low taxon sampling and the effect of evolutionary convergence. However, some interesting conclusions can be mentioned:
(1) Our study does not support the monophyly of Chaetarthriinae and neither of its two tribes. Larval characters place Guyanobius closer to Anacaenini than to Chaetarthriini, making further analysis necessary to test their tribal position.
(2) Larval characters are informative. Nonetheless, they are affected by derived or convergent morphologies related to different life strategies that generate topological problems.
(3) Different sources of characters are necessary (larval, adult, molecular) to generate robust phylogenetic hypotheses.
(4) Homoplasy partitioning seems to be an efficient strategy to analyze morphological data sets. The analysis implementing the homoplasy partitioning scheme proved to be more useful for solving some artifacts generated by convergent morphologies than the other alternative.
We thank Yûsuke Minoshima, an anonymous reviewer and Martin Fikáček for their valuable comments to improve the manuscript. This project received financial support from the Agencia Nacional de Promoción Científica y Tecnológica [Grant PICT–2017–1177] and from the University of Buenos Aires [Grant UBACyT–20020150100170BA]. CONICET (Consejo Nacional de Investigaciones Científicas y Tecnológicas, Argentina) is acknowledged for supporting research studies in the field of Systematics. The work of G. Rodriguez was supported by a postdoctoral scholarship from CONICET.
List of taxa studied for the analyses
Data type: .docx
Explanation note: List of taxa (genera and species) examined for the study and source of information.
List of characters and character states used in this study
Data type: .docx
Explanation note: Characters and states used in the phylogenetic analyses.
Data matrix (27×128) analyzed for this study
Data type: .nex
Explanation note: Chaetarthriinae TNT data matrix
Chaetarthriinae partitioning scheme and data matrix for the Bayesian inference analysis
Data type: .docx
Explanation note: Partitioning scheme and data matrix for the Bayesian inference analysis.
Chaetarthriinae most parsimonious tree with all synapomorphies mapped
Data type: .pdf
Explanation note: Most parsimonious tree with all synapomorphies mapped. Characters in black indicate unique transformations; characters in white indicate homoplasious transformations.