Systematic Entomology (2020), 45, 349–364 DOI: 10.1111/ .12400
The evolution of Zoraptera
YOKOMATSUMURA 1,2,ROLFG.BEUTEL 1*,JOSÉA.RAFAEL 3*, IZUMIYAO 4*,JOSENIRT.CÂMARA 5*,SHEILAP.LIMA 3 KAZUNORIYOSHIZAWA 4
1E G ,I ü Z Ev h ,F h S h U v J ,J ,G , 2D F M h B h ,Z I ,K U v ,K ,G , 3I N P A z ,M ,B z , 4S E ,S h A ,H kk U v ,S ,J 5U v F P í, B J ,P í, B z
Abstract. Z h .B w x wh h k w , w h h DNA - v h . Th h h w h Z v h , h w . Th h h h v h . Th v h P . P h h h Z w h v , h h . Th h h P , v h k G w L . Th x v f v h , h v , k h h v h .W v v h h v .O v / h , h k .
Introduction B et al., 2014; M h et al., 2014 ; Ch , 2018). I h h v ( v w Z h h I M h - M h et al., 2014 ;K et al., 2016; B et al., 2017), G . Th w h h w h Z (G &E , 2005; h P - v (Y h z w , 2011; M et al., 2014; C :Y k M ,E G ,I ü Z Ev h ,F h S h U v W &P , 2014; M h et al., 2014 , 2015; M J ,E . 1, 07743 J ,G &D F - et al., 2015; W et al., 2019). R ,W et al. M h B h ,Z I ,K (2019) h h h - U v , B h G 1–9, 24118, K ,G . P v v , E- : k . .h @ . ;R G. B , h h h w h M E G ,I ü Z Ev h , et al. (2014). Th v Z h F h S h U v J ,E . 1, 07743 J ,G . D , h w h E- : . @ - . ;J é A. R ,I N P A z ,C x P 2223, 69067-375 M , AM, h . Th h h - B z . E- : @ . v. ;K z Y h z w ,S P w ‘ - w E ,S h A ,H kk U v , 060-8589 w h f v h S ,J .E- : @ . .h k . . w ’(W et al., 2019). C h w h Z ( . .F h & B , 2008; ∗Th h h w k. M h et al., 2014 ;M et al., 2015),
© 2019 Th A h . Systematic Entomology h J h W &S L h R E S . 349 Th h h C v C A L , wh h , , v h w k . 350 Y. Matsumura .
h x v h - h h x v h h ‘ ’ . Th v h h h h v .H w v , w h w h x h f v h h k h h x (M h et al., 2014 ). h h v ( E , 2003). I h v - Th h h - ( . . Ph ,M ,B , w h Z . Th x O h ), 44 x 16 x v . Th v - Z (M h et al., 2018, 2019; h v v - Ch &S , 2019). K k vá-P k & P k (1993) x h h ( S w h Z h w v .H w v , et al., 2012). Th h v w h h h x k w v v w h v w h (Ch , 1989). C , h w z h . w h Zorotypus E (2000) wh ‘ h h - h ’.L k w , Ch & Ch (2000) w z w h Materials and methods Zorotypus (E , 2000). S h ,E ’ f h w (R &E , M h w h fx 2006; T & Wh , 2012; M h et al., 2013; Y w h 80–99.5% h (F . 1). T Zoroty- et al., 2015; W et al., 2016; Ch , 2018). Th pus novobritannicus w w h A h C - Zorotypus v , < 3 , ,B h Y U v ,P v , UT, U.S.A. I , v , . Th k 31 v 21–22 w w h h x v (F . 2). W h YK16-10 h ( h ) x v E Z. . 6. W (M h et al., 2014 ; Ch , 2018). C Z. huxleyi Z. hamiltoni h h P h , Z. . 6 h (W et al., 2019), Z h v .O w h z h , h v P ,H ,E h , z .H w v , h v O ,Z A h h . Th w h v w h A h h . Th h x w . G B k ( h Th k v - T S1, S2). h x h . Th h h v f h v v v , w h (Hü , 2007; M - DNA extractions, amplifcations, sequences and alignment et al., 2014), h w k x ( . .G , 1938). I , - h P h w w : w ( . .G , 18S RNA H 3, h 16S RNA 12S 1938; N w, 1978, 2000; M h et al., 2013). T RNA. Th k w 18S k w , h h P . (18S-Z - : 3′-ATT AAG CCA TGC AAG TGT CAG-5′; D h 18S-Z - : 3′-TTA RYA TAT GCT ATT GGW GCT GG-5′), k w w h Z , , , Z. zimmermani H 3 (H 3-E - : 3′-AAR GCY CCW MGM AAR (G , 1939) h Z. barberi (G , 1938). CAR CT-5′;H 3-E - : 3′-TGR ATR GCR CAV AGR TTR S (G , 1938; GTR TCY TC-5′), 16S (16S : 3′-CCG GTC TGA ACT CAG P , 1949, 1951; Hw , 1974, 1976; R &E , ATC ACG T-5′; 16S -L : 3′-CGC CTG TTT ATC AAA 2006; Hü , 2007; R et al., 2008; M h et al., AAC AT-5′) 12S (12S-Z - : 3′-TGG CGG YRW DWW 2013, 2018; W et al., 2016; K ˇá k et al., 2017; Y &L , RWT YTW TYR GRG G-5′; 12S-Z - : 3′-TTA CTM TYA 2017), k h f AAT CCA CCT TC-5′). M h DNA x , PCR .A h v f h f w Y h z w &J h h h , h (2008). S f w z h k ( . . h G -TE V G , 1938). Th v h - (P ,M , WI, U.S.A.) w - x .M .A - w h w h , - w w f h .R RNA h h wh h h w ma t 6.5 (K h & S , 2013) w h k w (Sh , 1978; Ch , 1994, 1995; M h et al., h Q-INS- , wh h 2011; D et al., 2013). Th w - h RNA .A w
©2019 Th A h . Systematic Entomology h J h W &S L h R E S . 45, 349–364 The evolution o Zoraptera 351
Fig. 1. Z . (A) Z. . C R ; (B) Z. asymmetristernum K ; (C–F) Z. caudelli M . Ph h T. K (A) T. K (B–F). [C f v w w . ].
, w x h w h x x . (F S1). P v h w h h h h Model selection and phylogenetic estimation ( . .K , 2004; Y h z w & J h , 2005; I h w et al., 2011; M et al., 2014; W Th h w et al., 2019). Th , w h h - partition inder 2.3.3 (L et al., 2017), h M et al., (2014) w h h h . Th H 3 W et al., (2019) h w h . ( h ) RNA ( h ) w f I , w h partition inder . Th -f h h h Z ( F S1).
©2019 Th A h . Systematic Entomology h J h W &S L h R E S . 45, 349–364 352 Y. Matsumura .
Fig. 2. C h h .D B z h w h .
W x k h iq-tree 1.6.3 v E (T 1). F , (N et al., 2015), w h 10 000 k - h Rh h (412 M ) w h h h w h - (H et al., 2018) x Ev et al. (2019). I h v .T h , , h h x 450 M w iq-tree w .A h - Z -P v M et al. , w h (2014) T et al. (2015). h F . 3. A B w F h mcmctree , w f h - mrbayes (R &H k, 2003). W h v 419 M h w h w h h 1 000 000 - P –P h T et al. , w v 1000 . Th (2015). B h , h f 10% w x - , 50% w baseml h paml w k . - w Th GTR + G w w h = 0.5, wh h w . tracer h beast w k (B k- x h et al., 2014) w h k h h M k v h M jmodeltest (P , 2008) h .W C (MCMC) h v . 1 000 000 , h v w v 50 . Th f 10% h v w Divergence time estimation x - .W w h k h h MCMC h v ( R F v , B h w et al., 2017). h w mcmctree h paml 4.8 w F h beast , w h clade ages k k (Y , 2007) beast 2.6 (B k et al., 2014). (M h et al., 2017). Th w w : Th w w BEAST M T h , x k M et al. (2014) T et al. (2015): 160 h k , h- h h .W M h v P ; 130 M h 20 , h f 10% v I ; 99 M h h v w x - . tracer h
©2019 Th A h . Systematic Entomology h J h W &S L h R E S . 45, 349–364 The evolution o Zoraptera 353
Fig. 3. C x k h iq-tree. N - w .A k h h w .M Z h h h ( x ). [C f v w w . ].
Table 1. A , - x - (DEC) ( L ;R &S h, 2008) h - F x C A (M ) w rasp 3.2 (Y et al., 2015). D -v Pronemoura angustithorax P 161.0–160.5 (DIVA; R , 1997) w v h Sorellembia estherae E 99.9 DEC .H w v , v h w h DIVA Valditermes brennenae I 136.4–130.0 w f w h x w h - v (K h, 2010). F v h w f :A beast w k (B k et al., 2014) w (AF), I (IM), N (NA), N (NT) h k h h MCMC h v . A . Th x w h w w , Biogeographical analysis w w w h . F x , h w A w h h . Th h h mcmctree .O h w h k w w x h .W h .
©2019 Th A h . Systematic Entomology h J h W &S L h R E S . 45, 349–364 354 Y. Matsumura .
Character evolution w h Z. asymmetristernum (AF). Th - h Z. .1 (AF) w h W h w h :( ) A + N (77.15%) A (22.85%) ;( ) (F . 4). ;( ) ;( v) C 2 3 w h v v 236 z h k; (v) M (179–295 M ) (F . 4), - ; (v ) z - h N (100%). C 3 9–11; (v ) f Z. barberi (NT) h , ; (v ) h h wh 2 h v v x (‘ ’ h ). Th v (F . 3). C 2 v f 183 M (134–238 v x , h - M ) (F . 4). Th w h w h .I , w x N (74.47%) h I + N O SZX12 (O - (25.53%) (F . 4). C 2 h C ,T k ,J ) - (F . 3). Th f 2 Z. weidneri .F v v w h v k (NT), Z. brasiliensis (NT) Z. huxleyi (NT) (F . 3), w h h v w w k L Z. weidneri Z. brasiliensis. Th M205 A w h L DFC420 h w w h v v 128 M (86–180 M ) las 3.8 (L M G H,W z ,G ).R v (F . 4) h N (F . 4). Th 2 h w h w- w h v 161 M (114–214 M ).O - :T x (1970), H et al. (2011) K et al. ( 2 ) v h N h h (2003). Ch v w w h h w ( 2 ) h I - mesquite 3.6 (M &M , 2018). + A (35.33%), I (33.21%), I + N (26.23%), h N (5.24%) (F 3,4). Th N Data accessibility ( 2 ) v 103 M (64–155 M ), Z. mexicanus (NA) 30 M (14–56 M )(F . 4). Th Z. mex- A v F S1. icanus w h N + N . Zorotypus novobritannicus (A ) w h I , h v w Results 138 M (94–190 M ). Th v 104 M (64–155 M ) h I (F . 4). Phylogeny, dating and biogeography Th v beast (F . S4) h w v . Th v Th 1753 ( wh h 75 h w h h h w x h ), h x mcmctree , wh h v k h (ML) B (F 3, S1–S3) w - 1 w .H w v , h x w k h. N h - v . , w h w h h h (M et al., 2014; W et al., 2019), h h w h Z Evolution o reproductive character states (F 3, S1–S3). Th , h h h- h v h , w B v v , h ML h . x , h h h - Th h h Z w w v [100% (BS), (PP) = 1) (F S1, h h z S3) v h (F . 3). C T S3. C h z z 1 fv : Z. hubbardi w v , h - (N : NA), Z. impolitus (I : IM), Z. shan- v h .A noni (N : NT), Z. asymmetristernum (A : AF), h , Z. . 1 (AF) (F . 3). Th h z B ’ (2018) f h v h Z 1 w v (F . 4). .A h C 1 h v 270 M (210–385 h (3) (6), h w M ) h v 224 M (163–285 M ) Z . (F . 4). W h 1, Z. hubbardi (NA) Z. impolitus (IM) Th ML w v - 155 M (89–225 M ) (F . 4), h h h h (F . 5). H - (F . 4) h v . Zorotypus h w , shannoni (NT) v 85 M (42–143 M ) v h (F . 5A). A 2
©2019 Th A h . Systematic Entomology h J h W &S L h R E S . 45, 349–364 The evolution o Zoraptera 355
Fig. 4. A h w - h Z h - x - (DEC) . T x k h .P h h h k h h .D h v F . S5 (ES9). [C f v w w . ]. w h k w h , h Th w h h 2 2 v .A - 1. f h v Th Z h P (H et al., 2007), - h k, h k w h (H h 2 + 3. I - et al., 2011; B , 2018). Th Z f v (F . 5C). w (F . 5B). M f h h
©2019 Th A h . Systematic Entomology h J h W &S L h R E S . 45, 349–364 356 Y. Matsumura .
Fig. 5. M x k h w h v h Z . [C f v w w . ].
©2019 Th A h . Systematic Entomology h J h W &S L h R E S . 45, 349–364 The evolution o Zoraptera 357
Fig. 5. C . [C f v w w . ]. k w h h h Z. v 2 3 shannoni (NT) + Z. asymmetristernum (AF) + Z. . 1 (AF) f .H w v , h w h h h 1 (F . 5D). I k h h v v 1 2 + 3. Th h h h , w h h h w h f 1, Z. asymmetristernum. v w v 2 + 3. Th h h Th h z v v v w h v (F . 5E), h h (F . 6). E v
©2019 Th A h . Systematic Entomology h J h W &S L h R E S . 45, 349–364 358 Y. Matsumura .
h 9–11, h v w z h . Th h h h . w , h v M 1, . . Z. hubbardi (NA), Z. impolitus h w (IM), Z. shannoni (NT), Z. .1 (AF) Z. asymmetristernum Z .V h w (AF), h , h 80–100 M (S et al., 2012). Th Z. hubbardi (NA) Z (F . 5F). Z. impolitus (IM) h J , wh Th k L x (S et al., 2012). Th 1 h h h .H w v , v h C , h f h Z. brasiliensis (NT, 2 ) w A + N , wh h Z. gurneyi (NT) h (S v , G w (S et al., 2012). Th k- P 1947; Ch , 1997). O - k h J C (100–160 .H w v , h w h k w M ;S et al., 2012), h x h , h w 1. Th Z. shannoni (NT) (F . 5G), w h h v v v - Z. asymmetristernum (AF) (85 M ) Z .C h h h h h v .A h h h N h v x k w Z. barberi (NT, 3) (Ch , 1995). A h c. 100 M (S et al., Th h k w v 2012), h v (T S3). A h h h f , .H w v , h h w w h x v h h h - h A Z. shannoni . Th w , h h h S h A O , h v k h (F . 5H). beast w v (24 M ). Th w 2 3 w c. 236 M , 2 v c. 183 M . Th f Discussion h h N Th f h h Z . Th h h G w h - L (S h et al., 2004; S et al., 2012). Th , z , v h w Y h z w v h h w h &J h (2005). T , h w - h P .C 2 h w h ( 2 , 2 , 2 ), 2 h Z :( ) h ( I A . Th - h );( ) f w v 161 M v 138 M .D h , h h w ;( ) w - w h h - h h I + A v ; ( v) / - G w , A , (B &G , h I 120 M (S et al., 2012). Th 2001; B et al., 2014; M h et al., 2014 ).H - h z k- - h Z. hubbardi (NA) (K z v .O w et al., 2002) h Z . h h C w h h - w k- .H w v , h h v P (W et al., 2019), wh h v - , h h , z x v h h .C , f h v h h h v - Z , h h z , - . Th x h ( k) wh Z. mexicanus (NA, 2 ), wh w 30 M . Th z x .O h h P -C R A h v h h v h Z . 60–90 M ( h h S et al., 2012). Th h Z. mexicanus (NA) v h S h A , wh h v C A Phylogeny, dating and biogeography h h A . Th P h z Th h x h h h v (Ch , x Z h . Th - 1994, 1995; D et al., 2013) w h v h P (F . 3) h v h h C (F . S5), wh h w (D et al., 2011, 2012, 2014 , , ). Th v P , x w h - x Z. impolitus (IM, 1) (D et al., G w L (S h et al., 2004). Th h - 2013) w h f . Th x 1 2 v h k k
©2019 Th A h . Systematic Entomology h J h W &S L h R E S . 45, 349–364 The evolution o Zoraptera 359
Fig. 6. M h v h v w. (A) Zorotypus hubbardi; (B) Z. . 1. C YK2; (C) Z. mexcanus; (D) Z. weidneri B z ;(E) Z. . 6 E . 1000–1200 YK10, Z. hamiltoni; (F) Z. huxleyi E ; (G) Z. cervicornis; (H) Z. caudalli; (I) Z. . 2 V . 1900 YK15; (J) Z. novobritannicus.S , 200 μ . [C f v w w . ].
©2019 Th A h . Systematic Entomology h J h W &S L h R E S . 45, 349–364 360 Y. Matsumura .
- h h - F h x , h h h , wh h v h P z h Zorotypus, . . Z. guineensis (AF, .S h v v h h ), w h v f . Th w h h , . . h v S v (1913) v , w x x D .S h f .D et al. (2014 ) - v h h (G S v ’ h h . Th et al., 2016). D et al. (2014 , ) h h f h k . v Z , h :( ) h A h h x , h f h w h D et al. (2011, 2012, 2014 , ) h - 1 G w h -C ( h - k 2 + 3. w v , . .P J , F h ,D et al. (2014 ) h h 1988; E &G , 2002; K , 2005); ( ) Z. caudelli v ( w h h ) (IM, 2 ), Z. magnicaudelli (IM, 2 ), Z. huxleyi (NT, 2 ) h Z. weidneri (NT, 2 ) h ; ( ) h Z. magnicaudelli (IM, 2 ), Z. caudelli (IM, 2 ) Z. huxleyi Z. shannoni (NT, 1), Z. hubbardi (NT, 1) Z. impolitus (NT, 2 ), h h Z. hubbardi (NA, 1) Z. impolitus (IM, 1) f .M h et al. (IM, 1). H w v , h h (2015) h 1. F , h h Z. Z. impolitus (IM, 1) Z. hubbardi (NA, 1). Th - guineensis v h Z. shannoni (NT, w h h - 1) ( S v , 1913; G , 1938), h h v h h . h v x. B h v h , Z. guineensis (AF) z . Th , w h x . Classifcation
A x Z w f h Morphological evolution , Zorotypus. Th , v h v - O h v v f .A , h h v h I ,K k vá-P k & P k (1993) h .F h x h w v h - v w, h v w (O v N w W ).H w v , O W h h Z. barberi (NT, 3) z w h , h - (G , 1938) h - h h h w w h Z (T S3). H w v , h (K k vá-P k & P k, 1993). I h v f x h h , Ch & Ch (2000) h h O W Z. caudelli (IM, 2 ), M - T w . Th x - et al. (2014), k h h w h K k vá-P k & P k (1993) Ch & Ch x, - h h v v v - (2000) h h - . Th x , f x K k & B (2006), h w h h [ . . Z. hubbardi (NA, 1)] h f ( h w (Hü , 2007). M v , h h k h x ) h h .O h w h v f f h h h Z h v v v h w . h f h .N v h , h Th h K k vá-P k & P k (1993) f . 2 2 w h k w .R ,R et al. F h x w , (2017) h Z. brasiliensis (NT, 2 ), . . Z. barberi (NT, 3), Z. brasiliensis (NT, 2 ), Z. caudelli wh w v k w , h (IM, 2 ) Z. hubbardi (NA, 1), h h h . Th h k K k vá-P k & P k h , w h z (1993). Th w h v .A h x , Z. gurneyi , , 1, Z. hubbardi (NA, 1), h (Ch , h w f h v 1997). A Ch (2018) v w, v h w .C 1 , xh v w . w h h w h Th , wh h h w . Th h h 2 + 2 .A - h , h h . f - v v - Th , w , R et al. h K k vá-P k & P k (1993). (2017).
©2019 Th A h . Systematic Entomology h J h W &S L h R E S . 45, 349–364 The evolution o Zoraptera 361
A h v v v 1. Th h h h h f h h . f .H w v , h v (T S3) Th k w Z h h w f 14 28 w h - .H w v , h h v h .I h w - , v .F , v h h w h h v h h w Z. hubbardi (NA, 1) Z. shannoni (NT, 1) , h , ( G , 1938). D h h v h , h , , v , v w , Z. hubbardi Z. caudelli h Z. guineensis. (Hü , 2007; M et al., 2014). A h h z - h , h z - - - h - , Author contributions (F h et al., 2014). N w w h h , YM, RGB, KY JAR, JTC z - v h v h . Th ; JAR, JTC, YM KY ; YM, IY , h h - KY x ;KY - , h h h ;YM KY v h ; . Th h h h h h . YM KY w h Z , w h - RGB, JAR, SPL, JTC IY v .A h v h , h w B v h f h . F T S3. M h et al. (2014 , ) h h Z. caudelli (IM, 2 ). Th , h h v v Supporting Information v . S v v w h A h v v h h v , h S I h h . h h k 9–11. P h h k Table S1. A h - h .A h h . BYUC, A h C ,B h k w , w k h k Y U v ,P v , UT, U.S.A.; INPA, N I - . Ex h x Z. impolitus A z R h, B z ; YK PC, Y. M (IM, 1), h k w h v h K U v., G . h h h w [Z. Table S2. M h . hubbardi: NA, 1 (G , 1938); Z. barberi: NT, 3 (Ch , 1995); Z. gurnery: NT, (Ch , 1994); Z. huxleyi Table S3. A h h k w Z. weidneri: NT, 2 (J.A. R et al., v ); h x .S h Z. caudelli: IM, 2 (M h et al., 2011); Z. magnicaudelli: h h h . IM, 2 (D et al., 2013)]. A h k w h h . Figure S1. U x k h - Th , h Z. impolitus h h iq-tree. M Z h h h v h k (M h et al., 2013), h h h w h ( h x ). h x (D et al., 2013). Th h k h h v , . . Figure S2. C B . Th h h h h h w - h . Th v f w M et al. (2014) W et al. v w .I (2019). , h h v Figure S3. U B . Tw Apachyus chartaceus (D :A h ) (Sh z & w h h w v M h , 2011), v w hwh h h . w h h z . A h h h h v x Z. barberi Figure S4. A - h Z - (NT, 3) h beast . (Ch , 1995). S f w v , fv 25 w h Figure S5. A h w v h (T S3). S - h Z h h h h v - x - (DEC) ;
©2019 Th A h . Systematic Entomology h J h W &S L h R E S . 45, 349–364 362 Y. Matsumura .
ML .P h h h T ó (CNP ):P x 457.423/2015–5; U - k h h .D v MCTI/CNP , 405.630/2016–6; B PQ, h . Th 300305/2007–9 300997/2016–7 JAR; PhD w h h w h F . 4. JTC ( 140983/2013–9 152131/2016–7) SPL ( 141371/2019–6). W k w File S1. N x f F çã A à P E A z x ( ) h , x (FAPEAM), P x, 062.00645/2017). k h (ML) B , h x Th h h . ML h h v . Ch - : (1) ; (2) - References ; (3) ; (4) - z h k; (5) ( B , R.G. & G , S.N. (2001) U h - ) ; (6) z z h x (A h ): v 9–11; (7) ; (8) v h . Journal o Zoological Systematics and Evolutionary Research, 39, 177–207. h h v x. F h h , w B , R.G., F h, F., G , S.-Q. & Y , X.-K. (2014) Insect h w : (1) k w :?, ( 1: Morphology and Phylogeny.W G G H&C , KG, h ): 1, ( 2: - h ): 2, : 0, B B . h ( : z + ): 3; (2) B , R.G., Y v k , M.I., M h , Y., F k , M. & M , k w : ?, : 1, : 0, h : K. (2017) Th h H x (A h ) h v v . Proceedings o the Arthropodan Embryological 2; (3) k w :?, : 1, : 0; (4) k w : ?, Society o Japan, 51, 1–15. : 1, v : 2, w h k : 3, B k , R., H , J., Küh , D., V h , T., W , C.H. et al. : 0, h : 4; (5) k w : ?, k w : (2014) BEAST2: w B v 1, k w : 0, h : 2, (6) k w :?, . PLoS Computational Biology, 10, 1003537. f : 1, h k : 2, : 0; (7) k w : B , B.E. (2018) A h h h H x (P ) v k - ?, f : 0, : 1, : 2, : , w h h h E . Arthropod Structure & 3, h ( z + ): Development, 47, 563–613. 4; (8) k w :?, : 1, : 0. Ch , R.F. & Ch , C.S. (2000) Formosozoros newi, w Z (I ) T w . Pan-Pacifc Entomolo- gist, 76, 24–27. Acknowledgements Ch ,X.&S , G. (2019) A w Zorotypus (I , Z ,Z ) h k w W h k T. K (K h U v ,J ), T. K h v Z h - h- (K U v ) N.O w (H kk U v ,J ) M . Journal o Zoological Systematics and Evolutionary v w h C ,C R Research, 57, 555–560. F h G , v . Y. M h (F k h U v - Ch , J.C. (1989) Zorotypus gurneyi, w , P ,J ), R. M h (T k U v ,J ),R.D Z. barberi G (Z :Z ). Annals (U v S ,I ) M. G (U v Gö - o the Entomological Society o America, 82, 149–155. ,G ) Z. impolitus , wh h - Ch , J.C. (1994) S x Zorotypus k w .YM h k Y. M h h gurneyi Ch (I :Z ) I. D h h z , T. Bü h (K U v ,G ) . Behavioral Ecology and Sociobiology, 34, 87–93. Ch , J.C. (1995) C h Zorotypus h Ph , S.N. G (K U - barberi (I :Z ). Animal Behavior, 49, 1511–1520. v ) h - Ch , J.C. (1997) Th v h Z : h .W h k T. K v x . The Evolution o Mating T. K h k h f , G.B h (FSU Systems in Insects and Arachnids ( . J.C. Ch B.J. C ), J ,G ), F.F. X v (I.N.P.A., B z ), M. M . 130–145. C U v P ,C . (K h U v ,J ),L.N (N M Ch , J.C. (2018) B v Z h -k w K ,K ), K.F (N k U v ,J ) . Insect Biodiversity: Science and Society, Volume 2 ( . h f . R.G. F P.H. A ), . 199–217. W -B kw ,N w W x f - J . : h G R h F D , R., G , M., M ,D.,M h , R., M h , Y., (DFG . MA 7400/1–1) h J S M , Y. & B , R.G. (2013) D v x Z : h P S ( w h , . . Naturwissenscha ten, 100, 581–594. 15 J03484) YM; KY h J S D , R., G , M., M ,D.,M h , R., M h , Y., h P S (24570093 15H04409) M , Y. & B , R.G. (2014 )G z h M x h U.S.A., h h : v v .A f h Zorotypus impolitus (I ,Z ). h C h N D v v C íf Arthropod Structure & Development, 43, 135–151.
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