A Proposed New Species Complex within the Cosmopolitan Ring Nematode Criconema annuliferum (de Man, 1921) Micoletzky, 1925
Abstract
:1. Introduction
2. Results
2.1. Species Delimitation Using Morphometry by Principal Component Analysis
2.2. Species Delimitation Based on Ribosomal and Mitochondrial DNA
2.3. Systematics
2.3.1. Criconema paraannuliferum sp. nov.
Description
Diagnosis and Relationships
Molecular Characterization
Type Habitat and Locality
Etymology
Type Material
2.3.2. Criconema plesioannuliferum sp. nov.
Description
Diagnosis and Relationships
Molecular Characterization
Type Habitat and Locality
Etymology
Type Material
2.4. Distribution of the Criconema annuliferum-Complex
2.5. Phylogenetic Analyses of the Criconema annuliferum-Complex
3. Discussion
4. Materials and Methods
4.1. Sampling Sites and Nematode Morphological Identification
4.2. DNA Extraction, PCR and Sequencing
4.3. Recognition of Putative Species within the Criconema annuliferum-Complex and Species Delimitation Approach
4.4. Phylogenetic Analyses
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Species | Sample Code | Locality, Province | Host-Plant | D2–D3 | ITS | 18S | COI |
---|---|---|---|---|---|---|---|
C. paraannuliferum sp. nov. | PR-129 | Calasparra, Murcia | peach | ON705053–ON705054 | ON705081–ON705084 | ON705034 | ON648825–ON648828 |
C. paraannuliferum sp. nov. | PR-125 | Barranda, Murcia | apricot | ON705055 | - | ON705035 | - |
C. paraannuliferum sp. nov. | PR-141 | Cieza, Murcia | almond | ON705056–ON705057 | - | - | - |
C. paraannuliferum sp. nov. | PR-203 | Ricla, Zaragoza | peach | ON705058–ON705059 | ON705085–ON705086 | ON705036 | ON648829–ON648830 |
C. paraannuliferum sp. nov. | PR-217 | Quinto de Ebro, Zaragoza | plum | ON705060–ON705061 | ON705088–ON705089 | ON705037 | ON648832–ON648835 |
C. paraannuliferum sp. nov. | PR-201 | La Almunia, Zaragoza | almond | ON705062–ON705063 | - | ON705038 | - |
C. paraannuliferum sp. nov. | PR-208 | Sástago, Zaragoza | apricot | ON705064 | ON705087 | ON705039 | ON648831 |
C. paraannuliferum sp. nov. | NEV-22 | Castillo de Locubín, Jaén | cultivated olive | ON705065–ON705066 | ON705094–ON705096 | ON705040–ON705044 | ON648840–ON648845 |
C. paraannuliferum sp. nov. | AR-086 | Prado del Rey, Cádiz | wild olive | ON705067–ON705070 | ON705090–ON705093 | ON705045–ON705047 | ON648836–ON648839 |
C. paraannuliferum sp. nov. | VAL-22 | Valdepeñas, Jaén | common yew | ON705071–ON705072 | ON705097–ON705102 | - | ON648846–ON648860 |
C. plesioannuliferum sp. nov. | VAL-22 | Valdepeñas, Jaén | common yew | ON705073–ON705080 | ON705103–ON705116 | ON705048–ON705051 | ON648861–ON648884 |
Character/Ratio a,b | MLC1 | MLC2 | MLC3 |
---|---|---|---|
L | −0.29 | 0.89 | −0.11 |
Stylet length | 0.00 | 0.66 | −0.11 |
R | 0.37 | 0.48 | −0.25 |
RV | 0.86 | −0.19 | 0.02 |
Ran | 0.90 | −0.23 | 0.26 |
a | −0.09 | 0.54 | 0.35 |
b | −0.30 | 0.61 | −0.17 |
c’ | 0.73 | 0.06 | 0.67 |
V | −0.12 | 0.15 | −0.53 |
SS loadings | 2.42 | 2.24 | 1.04 |
% of total variance | 0.27 | 0.25 | 0.12 |
Cumulative % of total variance | 0.27 | 0.52 | 0.63 |
Species | Gene | Intra/Inter a | P ID (Liberal) b | Clade Support c | Rosenberg’s PAB d |
---|---|---|---|---|---|
Criconema annuliferum | D2–D3 | 0.12 | 0.97 (0.87,1.0) e | 1.00 | 1.06 × 10−3 |
ITS | - | - | - | - | |
COI | 0.02 | 1.00 (0.95,1.0) | 1.00 | 5.3 × 10−16 | |
Criconema paraannuliferum sp. nov. | D2–D3 | 0.13 | 0.98 (0.95,1.0) | 1.00 | 7.1 × 10−9 |
ITS | 0.02 | 1.00 (0.95,1.0) | 1.00 | 2.4 × 10−6 | |
COI | 0.04 | 0.98 (0.93,1.0) | 1.00 | 6.5 × 10−0 | |
Criconema plesioannuliferum sp. nov. | D2–D3 | 0.09 | 0.98 (0.93,1.0) | 0.99 | 2.2 × 10−6 |
ITS | 0.02 | 1.00 (0.95,1.0) | 1.00 | 2.4 × 10−6 | |
COI | 0.01 | 1.00 (0.98,1.0) | 1.00 | 2.6 × 10−5 |
Locality | Calasparra, Murcia, Peach (PR-129) | Ricla, Zaragoza, Peach (PR-203) | Quinto de Ebro, Zaragoza, Peach (PR-217) | Valdepeñas, Jaén, Common Yew | Castillo de Locubín, Jaén, Cultivated Olive | Prado del Rey, Cádiz, Wild Olive | |||
---|---|---|---|---|---|---|---|---|---|
Character/Ratio a | Holotype | Female Paratypes | Fourth-Stage Juveniles | Females | Males | Females | |||
n | 1 | 20 | 4 | 5 | 5 | 11 | 8 | 5 439.4 ± 31.5 (409–490) | 8 |
L | 496 | 482.1 ± 34.9 (396–537) | 333.5 ± 48.5 (305–406) | 561.2 ± 61.8 (503–657) | 575.6 ± 33.3 (542–624) | 508.1 ± 45.4 (446–619) | 585.6 ± 18.9 (563–601) | 618.2 ± 21.7 (592–651) | |
R | 57 | 57.8 ± 0.8 (57–59) | 61.0 ± 0.8 (60–62) | 59.2 ± 1.3 (58–61) | 60.4 ± 1.9 (59–63) | 60.7 ± 2.6 (57–66) | 63.4 ± 1.1 (62–65) | - | 63.4 ± 1.1 (62–65) |
Rst | 12 | 13.5 ± 1.1 (12–15) | 16.0 ± 1.4 (15–18) | 13.2 ± 0.8 (12–14) | 13.6 ± 0.9 (13–15) | 14.1 ± 0.9 (12–15) | 13.4 ± 1.1 (12–15) | - | 12.8 ± 0.4 (12–13) |
Roes | 21 | 18.6 ± 1.8 (15–23) | 21.0 ± 2.4 (19–24) | 18.8 ± 0.8 (18–20) | 18.4 ± 1.1 (17–20) | 18.2 ± 1.2 (16–20) | 17.6 ± 1.1 (16–19) | - | 17.8 ± 1.6 (16–20) |
Rex | 20 | 17.8 ± 1.9 (14–22) | 20.0 ± 2.4 (18–23) | 17.8 ± 0.8 (17–19) | 17.6 ± 1.1 (16–19) | 19.0 ± 1.4 (17–21) | 18.8 ± 1.3 (17–20) | - | 18.8 ± 1.6 (17–21) |
RV | 7 | 8.5 ± 0.6 (7–10) | - | 8.8 ± 0.4 (8–9) | 8.8 ± 0.8 (8–10) | 9.1 ± 0.5 (8–10) | 8.4 ± 0.5 (8–9) | - | 8.2 ± 0.8 (7–9) |
Rvan | 3 | 4.3 ± 0.7 (3–5) | - | 4.4 ± 0.5 (4–5) | 4.6 ± 0.5 (4–5) | 4.4 ± 0.5 (4–5) | 4.2 ± 0.8 (3–5) | - | 4.4 ± 0.5 (4–5) |
Ran | 4 | 4.2 ± 0.6 (3–6) | 4.3 ± 0.5 (4–5) | 4.2 ± 0.4 (4–5) | 4.2 ± 0.4 (4–5) | 4.7 ± 0.5 (4–5) | 4.2 ± 0.4 (4–5) | - | 4.0 ± 0.7 (3–5) |
O | 10.6 | 9.7 ± 1.2 (8.2–13.3) | 10.8 ± 2.4 (8.0–13.2) | 8.9 ± 0.6 (8.3–9.8) | 8.9 ± 0.4 (8.3–9.5) | 11.2 ± 3.0 (8.6–14.4) | 8.4 ± 0.9 (7.5–9.1) | - | 8.5 ± 1.0 (7.8–10.3) |
a | 11.8 | 10.1 ± 0.9 (8.6–11.8) | 8.3 ± 0.6 (7.6–9.0) | 10.3 ± 0.6 (9.7–11.1) | 10.8 ± 0.5 (10.4–11.6) | 9.4 ± 0.6 (8.7–10.4) | 11.5 ± 1.1 (10.2–12.9) | 16.3 ± 1.8 (13.9–18.8) | 10.7 ± 1.5 (9.2–13.0) |
b | 3.4 | 3.5 ± 0.3 (3.0–3.9) | 3.0 ± 0.5 (2.6–3.5) | 3.9 ± 0.3 (3.5–4.4) | 4.1 ± 0.4 (3.8–4.8) | 3.6 ± 0.2 (3.2–3.9) | 3.9 ± 0.1 (3.7–4.1) | 4.5 ± 0.4 (4.0–4.9) | 4.0 ± 0.2 (3.6–4.2) |
c | 24.8 | 23.7 ± 1.5 (20.3–26.3) | 16.6 ± 1.4 (15.3–18.5) | 27.2 ± 2.5 (24.0–29.9) | 28.3 ± 2.5 (24.6–31.2) | 24.4 ± 2.0 (22.2–28.1) | 24.3 ± 1.2 (23.1–26.1) | 11.1 ± 0.8 (10.3–12.3) | 20.7 ± 3.2 (18.4–26.0) |
c’ | 1.1 | 1.1 ± 0.1 (1.0–1.2) | 1.1 ± 0.1 (1.1–1.2) | 1.1 ± 0.1 (1.0–1.2) | 1.1 ± 0.1 (1.1–1.2) | 1.1 ± 0.1 (1.0–1.2) | 1.1 ± 0.1 (1.0–1.2) | 2.0 ± 0.1 (1.8–2.1) | 1.3 ± 0.1 (1.2–1.5) |
V or T | 88.9 | 86.9 ± 1.6 (82.8–89.1) | - | 87.6 ± 2.0 (84.1–89.1) | 87.8 ± 0.6 (87.3–88.7) | 87.4 ± 1.5 (84.6–89.8) | 87.8 ± 0.5 (87.3–88.6) | - | 85.5 ± 1.4 (83.9–86.9) |
VL/VB | 1.7 | 1.8 ± 0.1 (1.6–2.0) | - | 1.7 ± 0.1 (1.6–1.9) | 1.8 ± 0.1 (1.6–1.9) | 1.6 ± 0.1 (1.4–1.8) | 1.8 ± 0.1 (1.7–1.9) | - | 1.7 ± 0.1 (1.5–1.9) |
First annulus | 15.0 | 18.0 ± 1.2 (15.0–20.5) | 12.6 ± 1.1 (11.5–14.0) | 18.0 ± 1.0 (17–19) | 19.6 ± 0.9 (19.0–21.0) | 18.7 ± 1.3 (16.5–21.0) | 19.1 ± 1.7 (17.0–21.0) | - | 19.7 ± 1.0 (18.0–20.5) |
Second annulus | 13.0 | 15.9 ± 1.0 (13.0–18.0) | 12.9 ± 0.9 (12.0–14.0) | 16.0 ± 0.7 (15–17) | 18.1 ± 0.7 (17.0–19.0) | 16.6 ± 1.3 (14.5–19.0) | 16.8 ± 2.0 (15.0–19.0) | - | 16.6 ± 1.1 (15.0–18.0) |
Stylet | 90.0 | 92.5 ± 3.2 (85.0–99.0) | 72.1 ± 4.9 (65.0–75.5) | 93.6 ± 4.2 (88.0–99.0) | 100.2 ± 6.8 (95.0–112.0) | 100.8 ± 5.7 (91.0–113.0) | 103.7 ± 3.0 (98.5–106.0) | - | 106.4 ± 8.1 (92.0–112.0) |
conus | 77.0 | 77.8 ± 3.1 (72.0–84.0) | 60.1 ± 5.3 (53.0–65.5) | 80.0 ± 2.7 (77.0–84.00) | 83.4 ± 6.6 (79.0–95.0) | 86.5 ± 3.8 (80.0–94.0) | 91.0 ± 3.2 (86.0–94.0) | - | 92.6 ± 6.1 (82.0–97.0) |
Pharynx | 148.0 | 138.0 ± 12.2 (115–168) | 111.3 ± 13.6 (91–119) | 145.4 ± 3.6 (140–150) | 141.8 ± 9.8 (130–157) | 142.5 ± 11.8 (132–172) | 151.4 ± 5.0 (146–159) | 97.8 ± 7.3 (85–102) | 155.8 ± 7.4 (148–168) |
Max. body width | 42.0 | 47.9 ± 3.0 (42.0–54.0) | 40.0 ± 3.6 (37.0–45.0) | 54.4 ± 4.5 (48.0–59.0) | 53.2 ± 2.8 (50.0–57.0) | 54.0 ± 4.8 (45.0–51.0) | 51.2 ± 6.1 (44.0–59.0) | 27.1 ± 2.3 (24.0–30.0) | 58.2 ± 6.3 (50.0–66.0) |
Anal body diam. | 18.5 | 18.7 ± 0.5 (17.0–19.0) | 17.5 ± 1.3 (16.0–19.0) | 18.8 ± 0.4 (18.0–19.0) | 18.7 ± 0.4 (18.0–19.0) | 19.0 ± 0.7 (18.0–20.0) | 22.1 ± 1.2 (23.0–25.0) | 19.8 ± 1.3 (18.0–21.0) | 22.5 ± 2.3 (19.0–25.0) |
Vulva to anus distance | 31.0 | 29.8 ± 1.5 (27.0–32.0) | - | 29.6 ± 1.7 (28.0–32.0) | 31.0 ± 1.0 (30.0–32.0) | 30.3 ± 2.1 (28.0–32.0) | 48.0 ± 5.8 (41.0–54.0) | - | 35.8 ± 6.0 (28.0–43.0) |
Tail | 20.0 | 20.4 ± 0.9 (18.5–22.0) | 20.0 ± 1.6 (18.0–22.0) | 20.6 ± 1.1 (19.5–22.0) | 20.4 ± 0.9 (20.0–22.0) | 20.8 ± 1.3 (19.0–23.0) | 24.1 ± 0.7 (23.0–25.0) | 39.8 ± 2.0 (38.0–43.0) | 30.4 ± 4.0 (24.0–34.0) |
Spicules | - | - | - | - | - | - | - | 33.1 ± 2.8 (30.5–37.0) | - |
Gubernaculum | - | - | - | - | - | - | - | 12.1 ± 1.8 (9.0–13.5) | - |
Character/Ratio a,b | Holotype | Paratypes | ||
---|---|---|---|---|
Females | Males | Fourth-Stage Juveniles | ||
n | 1 | 20 | 3 | 3 |
L | 489 | 460.1 ± 65.3 (372–658) | 340.7 ± 9.0 (332–350) | 302.0 ± 13.7 (287–314) |
R | 61 | 61.0 ± 2.6 (57–67) | - | 62.3 ± 1.5 (61–64) |
Rst | 15 | 14.6 ± 1.4 (12–18) | - | 16.7 ± 0.6 (16–17) |
Roes | 19 | 20.4 ± 1.0 (19–23) | - | 22.3 ± 0.6 (22–23) |
Rex | 20 | 20.1 ± 1.5 (17–22) | - | 20.3 ± 0.6 (20–21) |
RV | 11 | 10.4 ± 0.9 (9–12) | - | - |
Rvan | 1 | 1.5 ± 0.5 (1–2) | - | - |
Ran | 10 | 8.9 ± 0.8 (8–10) | - | 7.0 ± 1.0 (6–8) |
O | 9.2 | 10.4 ± 2.1 (8.9–17.0) | - | 9.8 ± 0.9 (9.3–10.8) |
a | 10.4 | 10.1 ± 1.0 (8.1–12.4) | 15.9 ± 0.7 (15.1–16.6) | 7.4 ± 0.3 (7.2–7.7) |
b | 3.6 | 3.3 ± 0.3 (2.7–4.0) | 3.6 ± 0.2 (3.4–3.8) | 2.9 ± 0.1 (2.8–2.9) |
c | 10.4 | 10.6 ± 1.2 (8.8–13.7) | 10.7 ± 1.0 (9.7–11.7) | 10.8 ± 0.9 (9.8–11.6) |
c’ | 1.7 | 1.6 ± 0.1 (1.3–1.8) | 2.0 ± 0.2 (1.8–2.3) | 1.2 ± 0.1 (1.1-1.3) |
V or T | 88.5 | 86.0 ± 1.5 (81.7–88.5) | 40.1 ± 4.1 (35.6–43.4) | - |
VL/VB | 1.8 | 1.7 ± 0.1 (1.6–2.0) | - | - |
First annulus | 15.0 | 16.2 ± 1.3 (14.0–19.0) | - | 10.7 ± 0.3 (10.5–11.0) |
Second annulus | 13.0 | 14.5 ± 1.1 (13.0–16.5) | - | 9.5 ± 0.5 (9.0–10.0) |
Stylet | 92.0 | 95.7 ± 5.7 (86.0–108.0) | - | 70.2 ± 5.3 (65.0–75.5) |
conus | 81.0 | 83.6 ± 4.6 (76.0–92.0) | - | 61.5 ± 3.8 (58.0–65.5) |
Pharynx | 134.0 | 139.8 ± 26.7 (103–215) | 94.0 ± 3.6 (90–97) | 105.3 ± 4.0 (101–109) |
Max. body width | 47.0 | 45.9 ± 6.8 (36.0–60.5) | 21.5 ± 0.9 (20.5–22.0) | 41.0 ± 1.0 (40.0–42.0) |
Anal body diam. | 27.0 | 27.0 ± 4.8 (22.0–39.0) | 15.7 ± 1.5 (14.0–17.0) | 23.7 ± 0.6 (23.0–24.0) |
Vulva to anus distance | 15.0 | 16.3 ± 2.6 (11.0–21.0) | - | - |
Tail | 47.0 | 43.9 ± 8.8 (33.5–66.0) | 32.0 ± 3.6 (29.0–36.0) | 28.0 ± 2.6 (26.0–31.0) |
Spicules | - | - | 31.0 ± 1.7 (29.0–32.0) | - |
Gubernaculum | - | - | 7.0 ± 0.5 (6.5–7.5) | - |
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Clavero-Camacho, I.; Palomares-Rius, J.E.; Cantalapiedra-Navarrete, C.; Castillo, P.; Liébanas, G.; Archidona-Yuste, A. A Proposed New Species Complex within the Cosmopolitan Ring Nematode Criconema annuliferum (de Man, 1921) Micoletzky, 1925. Plants 2022, 11, 1977. https://doi.org/10.3390/plants11151977
Clavero-Camacho I, Palomares-Rius JE, Cantalapiedra-Navarrete C, Castillo P, Liébanas G, Archidona-Yuste A. A Proposed New Species Complex within the Cosmopolitan Ring Nematode Criconema annuliferum (de Man, 1921) Micoletzky, 1925. Plants. 2022; 11(15):1977. https://doi.org/10.3390/plants11151977
Chicago/Turabian StyleClavero-Camacho, Ilenia, Juan Emilio Palomares-Rius, Carolina Cantalapiedra-Navarrete, Pablo Castillo, Gracia Liébanas, and Antonio Archidona-Yuste. 2022. "A Proposed New Species Complex within the Cosmopolitan Ring Nematode Criconema annuliferum (de Man, 1921) Micoletzky, 1925" Plants 11, no. 15: 1977. https://doi.org/10.3390/plants11151977