The Phylogenetic Relationships among Some Common Species of Amblyseiinae (Acari: Phytoseiidae) in China Orchard Based on the Mitochondrial CO1 Gene

Zhiwen Zou, Jianfei Xi, Fen Chen, Rui Xu, Tianrong Xin and Bin Xia*

College of Life Science, Nanchang University, Nanchang 330031, China

ABSTRACT

Amblyseiinae is the largest subfamily in Phytoseiidae, with more than 1,500 nominal species. However, the relationships of this subfamily was confused. In order to improve the classification system of Amblyseiinae, the mitochondrial CO1 gene sequence of seven Amblyseiinae species, collected from four provinces of China, were sequenced, and another seven Amblyseiinae species mt CO1 gene sequenced were download from GenBank. And the phylogenetic relationship between the Amblyseiinae genus and the subspecies was studied. The results showed that four species of Kampimodromus and two species of Euseius clustered into two different branches, but the branch of 8 species of Amblyseius and Neoseiulus was chaotic. It indicated that the species of Neoseiulus and Amblyseius should be assigned carefully. The results could not only reveal its phylogenetic relationship and provide molecular evidence for the evolution, but also provide a better way to identify phytoseiid species in citrus.

Article Information

Received 28 November 2017

Revised 01 March 2018

Accepted 24 April 2018

Available online 11 March 2019

Authors’ Contribution

BX designed the study. ZZ and JX carried out experiments and drafted the manuscript. FC and RX helped in sequencing. TX revised the manuscript.

Key words

Amblyseiinae mites, Mitochondrial CO1 gene, Phylogenetic relationships, Geographical populations, Classification system.

DOI: http://dx.doi.org/10.17582/journal.pjz/2019.51.2.763.772

* Corresponding author: xiabin9@163.com

0030-9923/2019/0002-0763 $ 9.00/0

Copyright 2019 Zoological Society of Pakistan

Introduction

China is an important source area of citrus, with many cultivars, such as Citrus unshiu, C. kinokuni, C. junos, C. ichangensis, C. sinensis, etc., being native to Southern China. Citrus are widely cultivated along the Jiangxi province, making it the largest producer of citrus in China (Ammerman et al., 1965).

Due to the rapid propagation and strong adaptability, agricultural pest mites have been a serious threat to citrus fruit, decreasing the quality and yield of crops (Xin, 1988). However, the widespread use of synthetic chemicals to control these arthropod pests indirectly results in death for a large number of their natural enemies. This diminishes the success of natural enemies as a natural means of population suppression for harmful mite pests.

Amblyseiinae (Acari: Phytoseiidae) (Krantz, 1978) often lives with predatory mites and phytophagous spider mites, eriophyoid, tarsonemid, aphids, coccid, and so on. It is one of the common natural enemies of harmful mites, and widely used as biological control agents (Wu et al., 2009; Xu et al., 2010). The artificial breeding and industrial production of some phytoseiid mites (such as Phytoseiulus persimilis Athias-Henriot, Neoseiulus fallacis Garman, Neoseiulus cucumeris Oudemans, Neoseiulus barkeri Hughes, Amblyseius eharai Amitai et Swirski, etc.) has been achieved (Mailloux et al., 2010). However, the phylogenetic system of phytoseiid has not been perfected, and the classification system of phytoseiini mites, especially the subfamily Amblyseiinae, is still unclear.

Amblyseiinae is the largest subfamily in Phytoseiidae, with more than 1,500 nominal species. The first described species of Phytoseiidae was Zercon obtusus Koch (Koch, 1839), which was named with Amblyseius obtusus. Amblyseius was first established as a genus in 1914, but was not initially accepted by many scholars (Berlese, 1914). Oudemans (1936) placed those species originally described by Berlese (1914) into Tyohlodromus. Vitzthum (1941) built the classification system of phytoseiini mites. Since that, Phytoseiini taxonomists confirmed Amblyseius and placed the species have setae Z2, Z4, Z1, S2, S4 and S5 short/minute, approximately subequal into this genus. Later, the subfamily Amblyseiinae was first built in 1961 and included 19 genera (Muma, 1961). This divided Phytoseiidae into 3 subfamilies: Phytoseiinae, Typhlodrominae and Amblyseiinae (Chant and McMurtry, 1994). A series of detailed reviews about Amblyseiinae (Chant and McMurtry, 2003a, b, 2004a, b, 2005a, b, c, 2006a, b) emerged from 2003 to 2006, which cataloged and/or described 1,499 species in 61 genera and 9 tribes.

Sequences of multiple genes or genomes have been used in phylogenetic studies in recent years and provided insights into the higher-level relationships in insects (Misof et al., 2014). Mitochondrial genomes, usually 16 kb in size with 37 genes for animals (Boore, 1999; Guo et al., 2017), have been shown to be a useful marker for inferring higher-level phylogeny (Bourguignon et al., 2015; Li et al., 2015).

In the past decade, the phylogeny of various mite groups has been studied using molecular markers such as mitochondrial (mt) gene (Dabert, et al., 2010), mt genome (Chen et al., 2014; Gu et al., 2014) and nuclear gene sequences (Kreipe et al., 2015; Pepato and Klimov, 2015). In this study, in order to improve the classification system of Amblyseiinae, the mitochondrial CO1 gene sequence of seven Amblyseiinae species, collected from four provinces of China, were sequenced. In addition, the phylogenetic relationship between the Amblyseiinae genus and the subspecies was studied. The results could not only reveal its phylogenetic relationship and provide molecular evidence for the evolution, but also provide a better way to identify phytoseiid species in citrus.

 

Materials and methods

Sample collection and identification

Seventeen geographic populations in Amblyseiinae were collected from Jiangxi, Guangdong, Hunan province, and Shanghai city, respectively (Table I; Fig. 1). Samples of each site were mounted as vouchers, using modified Berlese medium (Amrine and Manson, 1996) for morphological checking with a Zeiss A2 (microphoto camera AxioCam MRc) microscope. All of the specimens and vouchers were deposited in Department of Ecology, Nanchang University, China. Other samples were preserved in 70% ethanol at -20°C until DNA extraction.

 

Table I.- Sampled taxa for sequenced mt CO1 gene.

Families	Genus	Species	Location	Host	Code
Amblyseiinae	Amblyseius	A. eharai	Nanchang, Jiangxi	Citrus	AE1
			Xingan, Jiangxi	Tangerine	AE2
			Taihe, Jiangxi	Kumquat	AE3
			Yongxiu, Jiangxi	Citrus	AE4
			Guangzhou, Guangdong	Citrus	AE5
			Shanghai	Citrus	AE6
			Changsha, Hunan	Citrus	AE7
			Sihui, Guangzhou	Citrus	AE8
	Euseius	E. nicholsi	Nanchang, Jiangxi	Citrus	EN1
			Changsha, Hunan	Citrus	EN2
			Guangzhou, Guangdong	Citrus	EN3
		A. orientalis	Nanchang, Jiangxi	Citrus	AO1
			Xingan, Jiangxi	Chinese honey orange	AO2
		N. cucumeris	Guangzhou, Guangdong	Citrus	NC
	Scapulaseius	S. asiaticus	Nanxiong, Guangdong	Osmanthus fragrans	SA
		A. tsugawai	Jing 'an, Jiangxi	Citrus	AT
	Neoseiulus	N. barkeri	Ganzhou, Jiangxi	Navel orange	NB

 

Data collection

The mt genome sequences of seven species of Amblyseiinae and one outgroup species were retrieved from GenBank (Table II). The dataset includes four Kampimodromus, three Neoseiulus, and one Euseius mite species. The Metaseiulus occidentalis was used as outgroup.

 

Table II.- Sequences data for mt CO1 gene of some Amblyseiinae from GenBank.

Families / Genus		Species	Accession	Code
Amblyseiinae
	Kampimodromus	K. corylosus	EF372610	KC
		K. aberrans	EF372606	KA
		K. langei	EF372609	KL
		K. ericinus	EF372607	KE
	Neoseiulus	N. womersleyi	AB500133	NW
		N. californicus	AB500131	NCA
	Euseius	E. finlandicus	FJ404592	EF
Phytoseiinae
	Metaseiulus	M.occidentalis	EF221760	MO

DNA extraction, gene amplification and sequencing

 

The total DNA was extracted from a single adult mite using the improved Chelex-100 (Walsh et al., 1991). A 453-bp fragment of COI was initially amplified by PCR with the primer pair (Navajas et al., 1996), 5’- TGATTTTTTGGTCACCCAGAAG -3’ and 5’-TACAGCTCCTATAGATAAAAC -3’, then sequenced on an Illumina Hiseq 2000 platform at the Beijing Genomics Institute, Beijing.

Short PCRs were performed in 25-μL reactions containing: 2.5 μL of 10 × Buffer (Mg 2+ Free), 2.5 μL of MgCl2 (25mmol/L), 1.0 μL of dNTPs Mixture (10mmol/L), 1.0 μL of each primer(10mmol/L), 0.4 μL of Taq DNA polymerase (5U/μL), 5.0 μL of template DNA, and 11.6 μL water. PCR cycling conditions were: 5 min denaturation at 95 °C; 30 cycles of 1 min denaturation at 95 °C, 45 s annealing at 45 °C and 1 min extension at 72 °C; 5 min final extension at 72 °C; and then held at 4 °C. After amplification, 5 μL of the PCR reaction was analyzed by electrophoresis on a 1% agarose gel and visualized by GelRed staining. The PCR product was purified, then the strand of the amplified fragments CO1 were sequenced by Beijing Tiangen, Beijing.

Sequence and phylogenetic analyses

The DNAStar (Lasergene, v.7.1.0) was used for editing and assembling the raw data into sequence contigs. The fragment gene of mt CO1, was identified by BLASTn searches of NCBI based on highly conserved sequence motifs. Sequences obtained and cited from others published data were aligned using CLUSTAL W and numbers or parsimony-informative sites were calculated using MEGA5 software (Thompson et al., 1994). The base composition, nucleotide differences, transformation and transversion, genetic distance, etc. of the sequence were analyzed. All of the above analyses of the CO1 sequences were conducted using MEGA version 5 software (Tamura et al., 2011).

Phylogenetic analysis using the CO1 DNA fragment data was conducted using the Bayesian tree estimate methods and the Maximum likelihood (ML) method with 1,000 bootstrap replicates. Sequences for Metaseiulus occidentalis was used as a single outgroup. Maximum likelihood (ML) trees of the mt DNA genes was constructed with Paup* (v.4. ob.10; Swofford, 2002). The default parameters were used and the confidence values of the ML tree were evaluated via a bootstrap test with 1000 iterations (Felsenstein, 1985). Nodes supported by bootstrap values (BSP) ≥ 70% were considered strongly supported (Hillis and Bull, 1993). The Bayesian inference (BI) analysis using MrBayes version 3.12 (Ronquist and Huelsenbeck, 2003) was conducted using phylogeny. The dataset was run for 3 million generations, with tree sampled every 100 generations. After 2.5 million generations, the average standard deviation was below 0.01 in most Bayesian trees. The consensus tree was edited with FigTree1.4.0. Nodes supported by posterior probabilities (BPP) P 95% were considered strongly supported.

 

Results

mt CO1 gene sequence

The CO1 sequence of seven species in Amblyseiinae were sequenced in this study. All sequences were 453 bp long. The base compositions are shown in Tables III and IV. In the 17 geographic populations, average content of T (42.4%) is the most abundant. C content is the lowest (13.4.0%), and T content of SA (45.9%) is the highest while that of NB is the lowest (37.1%). C content ranges from 18.3% (NB) to 18.7% (NC). A+T content is higher than 70% within 8 AE geographic populations (AE1~AE8), and is less than 70% in the others, which shows a difference in different geographic populations.

Sequence variable sites

The 242 conservative sites, 211 variable sites and 173 parsimony informative sites were detected in the CO1 gene fragment of 14 species in Amblyseiinae, while 262 conservative sites, 191 variable sites and 150 parsimony informative sites were detected in 7 species of this study.

There were 411 conservative sites, 42 variable sites and 9 parsimony informative sites, among 8 geographic populations of AE (AE1 ~ AE8); 427 conservative sites, 26 variable sites and no parsimony informative site for the three geographic populations of EN (EN1~EN3); 443 conservative sites, 10 variable sites and no parsimony informative site detected for 2 geographic populations of AO.

 

Table III.- The content of COI gene of seven species in Amblyseiinae.

Species*	COI
	T/%	C/%	A/%	G/%	A+T/%	Total
AE1	41.3	15.0	29.8	13.9	71.1	453.0
AE2	41.7	14.6	30.2	13.5	71.9	453.0
AE3	41.3	15.0	30.0	13.7	71.3	453.0
AE4	41.9	14.3	30.0	13.7	71.9	453.0
AE5	41.5	13.9	30.7	13.9	72.2	453.0
AE6	41.9	14.3	30.2	13.5	72.1	453.0
AE7	41.9	14.3	29.6	14.1	71.5	453.0
AE8	41.5	13.9	29.8	14.8	71.6	453.0
EN1	43.3	11.9	26.0	18.8	69.3	453.0
EN2	44.2	11.5	25.4	19.0	69.6	453.0
EN3	42.8	12.4	26.0	18.8	68.8	453.0
AO1	43.0	11.5	26.0	19.4	69.0	453.0
AO2	42.8	11.7	26.0	19.4	68.8	453.0
NC	44.2	11.3	25.4	19.2	69.6	453.0
SA	45.9	11.7	23.6	18.8	69.5	453.0
AT	43.3	13.2	26.3	17.2	69.6	453.0
NB	37.1	18.3	29.8	14.8	66.9	453.0
Avg.	42.4	13.4	27.8	16.4	70.2	453.0

*For full names of species, see Table I and II.

 

Table IV.- Nucleotides composition of COI gene partial sequences of the 17 populations in Amblyseiinae.

Species	First base frequency (%)					Second base frequency (%)					Third base frequency (%)
	T-1	C-1	A-1	G-1	Pos#1	T-2	C-2	A-2	G-2	Pos#2	T-3	C-3	A-3	G-3	Pos#3
AE1	37	10.5	32.9	19.7	152.0	44	20.7	16.0	19.3	150.0	43	13.9	40.4	2.6	151.0
AE2	37	10.5	32.9	19.7	152.0	44	20.7	16.7	18.7	150.0	44	12.6	41.1	2.0	151.0
AE3	37	10.5	32.9	19.7	152.0	44	20.7	16.0	19.3	150.0	43	13.9	41.1	2.0	151.0
AE4	38	9.9	32.9	19.7	152.0	44	20.7	16.0	19.3	150.0	44	12.6	41.1	2.0	151.0
AE5	39	8.6	32.2	20.4	152.0	44	20.7	16.0	19.3	150.0	42	12.6	43.7	2.0	151.0
AE6	38	9.9	32.9	19.7	152.0	44	20.7	16.0	19.3	150.0	44	12.6	41.7	1.3	151.0
AE7	38	9.2	32.2	20.4	152.0	44	20.7	16.0	19.3	150.0	44	13.2	40.4	2.6	151.0
AE8	39	8.6	32.2	20.4	152.0	44	20.7	16.0	19.3	150.0	42	12.6	43.7	2.0	151.0
EN1	33	9.9	31.6	25.7	152.0	43	21.3	15.3	20.0	150.0	54	4.6	31.1	10.6	151.0
EN2	35	7.9	31.6	25.7	152.0	43	21.3	15.3	20.0	150.0	54	5.3	29.1	11.3	151.0
EN3	34	8.6	31.6	25.7	152.0	43	21.3	15.3	20.0	150.0	51	7.3	31.1	10.6	151.0
AO1	34	8.6	32.2	25.0	152.0	44	20.7	14.7	20.7	150.0	51	5.3	31.1	12.6	151.0
AO2	34	8.6	32.2	25.0	152.0	43	21.3	14.7	20.7	150.0	51	5.3	31.1	12.6	151.0
NC	36	7.2	28.9	28.3	152.0	44	20.7	15.3	20.0	150.0	53	6.0	31.8	9.3	151.0
SA	35	10.5	28.9	25.7	152.0	45	20.0	15.3	20.0	150.0	58	4.6	26.5	10.6	151.0
AT	36	7.9	31.6	24.3	152.0	44	21.3	16.0	18.7	150.0	50	10.6	31.1	8.6	151.0
NB	27	15.1	36.2	21.7	152.0	43	21.3	16.7	18.7	150.0	41	18.5	36.4	4.0	151.0
Avg.	35	9.6	32.1	22.9	152.0	44	20.9	15.7	19.6	150.0	48	9.9	35.6	6.5	151.0

*For full names of species, see Table I and II.

 

Genetic distance analysis

Genetic distance is shown in Table V. The results indicated that the intraspecific genetic distance ranged from 0.003 to 0.116 in 8 geographical populations of AE, of which had the smallest genetic distance was between AE2 and AE3, and AE2 and AE4, whereas the largest was between AE7 and AE8.

The intraspecific genetic distance ranged from 0.016 to 0.062 in 3 geographical populations of EN, of which the smallest genetic distance was between EN1 and EN3 and the largest one between EN2 and EN3. The intraspecific genetic distance between 2 geographical populations of AO was 0.015. The interspecific genetic distance between KC and KE was the smallest (0.119), whereas the largest was 0.429 between NCA and NW.

Phylogenetic tree

Figures 2 and 3 shoe that the topological structure of phylogenetic trees constructed based on the two different phylogenetic analyses are the same. Samples of Neoseiulus, Amblyseius, Scapulaseius, Kampimodromus and Euseius are isolated from the outgroup Metaseiulus occidentalis (statistical value is 0.98). Likewise, N. barkeri and N. womersleyi were recovered separate from the other taxa (statistical value is 0.59).

 

Table V.- Pairwise distances and transition/transversion (above the diagonal) based on COI gene.

 

Four species of Kampimodromus and two species of Euseius are clustered into two different branches. KC and KE, KL and KA had close genetic relationship in Kampimodromus, whereas SA had close genetic relationship with Neoseiulus and Amblyseius.

The branch of 8 species of Amblyseius and Neoseiulus was chaotic, in which NB clustered into a branch with NW and isolated with others. AT and NCA clustered into a branch firstly and then gathered together with AO. NC had close genetic relationship with SA. It was the same for the branch conditions of the phylogenetic trees constructed by ML analysis and BI analysis, the trend was generally consistent.

It could be known from the branch of 5 genera of ingroup that the geographic populations of AE (AE1~AE8), EN (EN1~EN3) and AO (AO1 and AO2) clustered into a clade, respectively. As the phylogenetic tree constructed based on 2 different methods revealed that within EN, EN1 had closer phylogenetic relationships with EN3 compared with the EN2. The phylogenetic relationship within 8 geographical population of AE, AE2, AE3 and AE4 are close in Jiangxi province.They are also close between AE5 and AE8 in Guangdong province.

 

Discussion and Conclusion

The different geographical populations of A. eharai, E. nicholsi and A. orientalis were showed a certain degree of genetic differentiation. Based on the genetic distances and phylogenetic trees, the phylogenetic relationships between the populations agreed with their geographic distribution. Many studies have shown that geologic diversity will result in significant genetic variation among different populations, especially in populations of Amblyseiinae, that lack strong migratory ability (Ma et al., 2010; Meng, 2008).

The precise identification in Phytoseiidae is difficult due to little effective morphological features required to distinguish the closely related species. Therefore, there is not a perfect classification system to date for the family, subfamily, or genus in Phytoseiidae which is recognized by most taxonomists (Athias-Henriot, 1977, 1978; Tsolakis et al., 2012).

Four species of Kampimodromus in this study have been clustered into one branch, as well as two species of Euseius, which fit their morphological system. The adscription of the classification of Amblyseius and Neoseiulus has, however, been confusing for a long time. The genera were erected in 1914 and 1948, respectively, but the researchers took a long time to accept these within the taxonomic community. Moreover, there were some taxonomists that had different opinions on the classification. Neoseiulus was topically merged into Amblyseius or another genus (Muma, 1961; Wainsstein, 1962; Schicha, 1987), but after the 1990s, Amblyseius and Neoseiulus were treated as two independent genera and eventually (Moraes et al., 2004) divided into different subtribes, Neoseiulini (Chant and McMurtry, 2003a) and Amblyseiini (Chant and McMurtry, 2004). Wu et al. (2010) did not adopt this system and instead divided Amblyseius into two subgenera, Amblyseius and Neoseiulus, respectively. For instance, N. barkeri was merged into Amblyseius (Wu, 1980a), then recombined with Neoseiulus (Wu, 1986). However, it was regarded as a member of two genera by different scholars at the same time (Chant and McMurtry, 2003; Wu et al., 2009). N. cucumeris was also rearranged several times, which was firstly placed into Amblyseius (Chant, 1959), then was divided into Typhlodromopsis (Muma, 1961), but later was replaced in Neoseiulus in 1986 (Moraes et al., 1986). A. tsugawai and A. orientalis followed the same process, from Amblyseius (Amblyseiinae) to Typhlodromus (Typhlodrominae) (Hirschmann, 1962), and then shifted back to Amblyseius again (Chant and McMurtry, 1994; Moraes et al., 1986). S. asiaticus was grouped with Typhlodromus (Evans, 1953), then to Amblyseius and Neoseiulus, and ultimately to Scapulaseius (Wu, 1980b; Wu et al., 2010). Similar to their complex morphological taxonomic relationship, the molecular evolutionary relationship was also unclear in the present paper. They did not cluster into single group. A. tsugawai, A. orientalis, S. asiaticus, N. cucumeris and N. californicus were clustered with three Euseius species, while N. womersleyi, N. barkeri and A. eharai were far away with other phytoseiid mites. Judging from our results, the species of Neoseiulus and Amblyseius should be assigned carefully. In fact, the two genera were differentiated only based on whether the length of Z5 seta was longer than the half width of dorsal plate or not (Wu et al., 2009). More molecular data would be helpful to distinguish the two genera.

 

Acknowledgement

The research was funded by the National Natural Science Foundation of China (31860601, 31460553), Natural Science Foundation of Jiangxi Province (20151BAB204016 and 20161BBF60066), funds from Jiangxi Food and Drug Administration (2017YX19) and Foundations from the Administration of Science and Technology in Nanchang City to Zhiwen Zou (2010NYZZ037, 2013HZCG008). We would like to thank Dr. Alexandra G Duffy (Brigham Young University, USA) for her support and comments on writing.

 

Statement of conflict of interest

Authors have declared no conflict of interest.

 

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