Research Article |
Corresponding author: Lucie Vaníčková ( luci.vanickova@gmail.com ) Academic editor: Teresa Vera
© 2015 Lucie Vaníčková, Vicente Hernández-Ortiz, Iara Sordi Joachim Bravo, Vanessa Dias, Alzira Kelly Passos Roriz, Raul Alberto Laumann, Adriana de Lima Mendonça, Beatriz Aguiar Jordão Paranhos, Ruth Rufino do Nascimento.
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:
Vaníčková L, Hernández-Ortiz V, Bravo ISJ, Dias V, Roriz AKP, Laumann RA, Mendonça AL, Paranhos BAJ, do Nascimento RR (2015) Current knowledge of the species complex Anastrepha fraterculus (Diptera, Tephritidae) in Brazil. In: De Meyer M, Clarke AR, Vera MT, Hendrichs J (Eds) Resolution of Cryptic Species Complexes of Tephritid Pests to Enhance SIT Application and Facilitate International Trade. ZooKeys 540: 211-237. https://doi.org/10.3897/zookeys.540.9791
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The study of the species complex Anastrepha fraterculus (Af complex) in Brazil is especially important in a taxonomical, evolutionary and pest management context, because there are evidences that some of them may occur in sympatry. In this review, we analyzed the main results supporting evidences that three cryptic species occur in Brazil. The taxonomical and phylogenetic relationships based on eggshell morphology, adult morphometrics, as well as cytotaxonomy and genetic differentiations are discussed. We also review available information on sexual behavior including acoustic communication of males during courtship and sexual incompatibility; and chemical signals involved in the communication between sexes, with a special focus on sex pheromones. We examined the role of long- and short-range pheromones (male-produced volatiles and cuticular hydrocarbons, respectively), their implications in sexual isolation, and their possible use for chemotaxonomic differentiation of the putative species of the Af complex.
South American fruit fly, cryptic species, taxonomy, sexual behavior, chemical communication, acoustic communication
The fruit fly Anastrepha fraterculus constitutes a complex of cryptic species (Af complex) currently composed of eight taxonomically recognized morphotypes (
Here, we present a revised synthesis on the current status of our knowledge of the A. fraterculus complex in Brazil, focusing on divergence among Brazilian populations by evaluating multiple aspects: (i) taxonomy and relationships, (ii) sexual behavior and reproductive incompatibility, and (iii) chemical communication between sexes.
The first documented evidence of a cryptic species complex appeared in the comprehensive taxonomic revision of the genus Anastrepha by
Since then, enough information has been gathered to affirm that the nominal species Anastrepha fraterculus in fact represents a cryptic species complex (Af complex). Some studies conducted in the 1990’s correlated morphological traits and genetics of Brazilian samples (
The historical taxonomy of the genus Anastrepha is largely based on adult characters of the female aculeus, external morphology of the body, and the wing pattern (
Adult female Anastrepha fraterculus (A) and typical forms of the aculeus tip and the wing pattern of morphotypes Brazilian-1 (B, E), Brazilian-2 (C, F), Brazilian-3 (D, G), respectively. (The photo of adult was made by Dr. Hoskovec, the images of aculeus and wings were modified from
Taxonomic studies of the nominal A. fraterculus (sensu lato) done by
Besides, morphometric assessment proved to be useful for the recognition of Anastrepha species.
However, based on adult morphology, the first evidence of differences among Brazilian populations of the Af complex from other countries was made with comparisons of seven samples from Mexico, two from Brazil (São Paulo and Piracicaba), and each one from Argentina (Tucumán) and Colombia (Tolima) (
Further morphometric analyses using 32 populations from Mexico, Central America, and South America (including Venezuela, Colombia, Ecuador, Peru, Brazil and Argentina), confirmed previous findings and clearly added that within the Af complex seven morphotypes could be discerned throughout the Neotropical region (
Differences in egg morphology discovered between Brazilian populations of the Af complex suggested the existence of two different taxonomic entities for the first time. Through scanning electron microscopy,
Scanning electron micrographs of the anterior tip (dorsal view) of eggs from Brazilian-1 (A), Brazilian-2 (B), Brazilian-3 (C) morphotype of Anastrepha fraterculus. The arrow shows aeropyles. Bars = 20 µm (A, B) and 50 µm (C). The images were modified from
Concerning the species distribution and host use of the Brazilian members of the complex, there is very limited information and few inferences can be made. For example, two species of the Brazilian complex, A. sp.1 and A. sp.2 exhibited preferentially an allopatric distributional pattern. However, in most of 18 locations sampled from Brazilian Inland Plateau, they can be found together infesting guavas (Psidium guajava) and oranges (Citrus sp.), respectively, and only two locations in the Paraíba valley (Santa Isabel and Jambeiro, in the state of São Paulo) recorded the co-occurrence of the three Brazilian forms (
Map of Brazil indicating the geographic locations from which Brazilian-1 (green), Brazilian-2 (blue) and Brazilian-3 (yellow) morphotypes of Anastrepha fraterculus were collected. 1 Parnamirim, RN 2 Maceio, AL 3 Conceição de Almeida, BA 4 Parati, RJ 5 Ubatuba, SP 6 Caraguatatuba, SP 7 Ilhabela, SP 8 São Sebastião, SP (region of sympatry of Brazilian-2 and Brazilian-3 morphotypes,
The first cytological evidence of differences between samples of the Af complex was reported by
Later
More recently,
The first molecular study of intraspecific variation in the Af complex in Brazil was performed by
A similar isozymic analysis conducted by
Studies of mitochondrial DNA (
Recently,
Unfortunately, available data as a whole do not permit correlating different karyotypes or genetic and molecular traits, with the morphology and distribution of the Brazilian sibling species, mainly because studies were carried out with flies from different locations. A synthesis of molecular datasets from the existing literature is precluded because the original authors applied different methodologies or genetic loci to analyse A. fraterculus samples (
The lek polygyny mating system displayed by A. fraterculus was first described by
Overall, time of mating and the period in which Af complex males from the studied Brazilian populations display their courtship behavior in leks seem to occur mainly in the morning, shortly after the sunrise (
Lek formation and courtship displays were compared among five Brazilian populations of the Af complex from South (Bento Gonçalves, Pelotas, and Vacaria – Rio Grande do Sul; São Joaquim – Santa Catarina) and Southeast regions of Brazil (Piracicaba – São Paulo) by
Although Brazil is the South American country with the highest number of Af complex entities (
Although some progress has been made toward our understanding about the reproductive isolation barriers among the Brazilian populations of the Af complex, this advance is still discrete given the high cryptic species diversity that could be potentially found in the north, northeast, south, and southeast of Brazil. Further studies need to be conducted in order to elucidate the mechanisms involved in the divergence among the cryptic species of the Af complex, which could help to predict their distribution.
Acoustic communication during reproductive behavior has been identified in twenty-four species of tephritid flies and characterized in ten species, including some Anastrepha spp. (
Intra- and interspecific variations in sound production may be important in the eventual reproductive isolation of species/populations and could contribute to speciation.
Future work should test the role that acoustic communication plays on the reproductive behavior and also if the temporal (time components) and spectral (frequency and intensity components) characteristics could be used in species/populations recognition. In addition, vibratory substrate-borne components of acoustic signals could transmit information between individuals; this possibility has not yet been studied in tephritid flies.
Sex pheromones play an important role in species/partner recognition and in the mating behavior of Anastrepha species (
A subsequent study carried out by
Further studies on the chemical composition of sexual pheromone of A. fraterculus and its perception by conspecific females were conducted (
A recent study on chemical and electrophysiological analyses and behavioural bioassays was performed using a population of A. fraterculus from Alagoas (A. sp.3, Alagoas, Brazil) revealing the presence of 29 compounds in headspace samples of A. fraterculus males (
The results of the multivariate principal component analysis (PCA) of the sex pheromone of the males of Anastrepha fraterculus from 7 different populations representing two Brazilian morphotypes (A. sp.1, A. sp.3). A. sp.1. PEL – Pelotas (RS, BR), BEN – Bento Gonçalves (RS, BR), VAC – Vacaria (RS, BR), SAO - São Joaquim (SC, BR), TUC – Tucumán (AR); A. sp.3. AL – Alagoas (AL, BR); PIRA – Piracicaba (SP, BR) [modified after
Chemicals identified in the male sex pheromone mixture of Anastrepha fraterculus Brazilian morphotypes: A. sp.1 PEL – Pelotas (RS, BR), BEN – Bento Gonçalves (RS, BR), VAC – Vacaria (RS, BR), SAO – São Joaquim (SC, BR), TUC – Tucumán (AR); A. sp.3. AL – Alagoas (AL, BR) [modified after
No. | Compound | RI | A. sp.1 PEL | A. sp.1 BEN | A. sp.1 VAC | A. sp.1 SAO | A. sp.1 TUC | A. sp. PIR | A. sp.3 AL |
---|---|---|---|---|---|---|---|---|---|
1 | p-Cymene | 1022 | ++++ | + | ++ | ++ | ++ | + | +++ |
2 | 2-Ethylhexan-1-ol | 1029 | + | +++ | ++++ | + | ++ | + | tr |
3 | Limonene† | 1041 | ++++ | ++ | +++ | ++++ | +++ | + | ++++ |
4 | (Z)-β-Ocimene | 1050 | ++ | + | tr | ++ | +++ | +++ | - |
5 | Nonanal | 1107 | + | ++ | ++++ | ++ | tr | + | + |
6 | (Z)-3-Nonen-1-ol† | 1159 | tr | ++ | + | + | ++ | + | + |
7 | (E, Z)-3,6-Nonadien-1-ol† | 1161 | tr | ++++ | + | +++ | +++ | ++++ | ++++ |
8 | Decenal | 1210 | ++ | + | ++ | + | tr | + | + |
9 | (Z, E)-α-Farnesene† | 1495 | + | + | + | ++ | + | + | + |
10 | Germacrene D | 1498 | + | + | + | + | tr | + | + |
11 | (E, E)-α-Suspensolide | 1506 | ++ | ++ | + | ++ | ++ | ++ | ++ |
12 | (E, E)-α-Farnesene† | 1512 | ++ | ++ | + | ++++ | ++++ | ++++ | + |
13 | Anastrephin | 1617 | + | + | + | + | + | + | + |
14 | Epianastrephin† | 1621 | ++ | ++ | + | +++ | + | ++ | + |
Further comparison of the male-borne chemical profiles of seven populations of A. sp.1 [Bento Gonçalves (Rio Grande do Sul), São Joaquim (Santa Catarina), Pelotas (Rio Grande do Sul)], A. sp.3 (Alagoas), and Andean (Duitama, Ibague, Sibundoy) morphotypes confirmed the previous findings on variability among male pheromone composition (Vaníčková et al. 2015). Male-specific compounds, which were proved by
Although long range attractants (sex pheromones) are essential for male and female flies to find each other, other substances, including cuticular hydrocarbons (CHs), may function as short range attractants and/or agents which trigger physiological changes, such as induction of receptivity in females and other behaviors associated with mating (
Study of sex- and age-dependent differences in CHs production has been conducted for a laboratory population of A. fraterculus (A. sp.1, Tucumán, Argentina). It was found that sexually mature males had specific unsaturated hydrocarbons (7-monoenes) on their cuticles, which are absent in females (
Nevertheless, when compared the chemical profiles of males and females CHs from A. sp.1 [Bento Gonçalves (Rio Grande do Sul), Pelotas (Rio Grande do Sul), São Joaquim (Santa Catarina)], A. sp.3 (Alagoas) and Andean morphotype (Duitama, Cachipay, Sibundoy), CHs were found to have a limited use for distinguishing between A. sp.1 and A. sp.3 (Vaníčková et al. 2015). In all, the seven A. fraterculus populations analyzed formed two main clusters presenting Andean and Brazilian entities. The A. sp.1 and A. sp.3 populations created monophyletic cluster. These results point out that the relationships between the CH profiles and geographical isolation and/or influence of diet, host fruit, laboratory rearing and possible genetic variability are very complex and not yet understood among the Af complex. Therefore, it is necessary to conduct future studies, which will elucidate these complicated relationships of the CH chemical profiles and evaluate their use as specific taxonomic markers. The Brazilian-2 morphotype (A. sp.2) should be also examined for the CH composition and compared with the A. sp.1 and A. sp.3 morphotypes.
To date, three sibling species have been documented from the Af complex in Brazil. This complex work has relied on a number of analytical methods, such as differences in karyotypes (
The three Brazilian species exhibit conspicuous differences in the sex chromosomes, both in terms of size and the amount and arrangement of heterochromatic blocks (
Out of the eight morphotypes currently recognized within the Af complex, there is compelling evidence that Brazilian morphs are the only ones to occur in sympatry in certain regions of the country. For instance, the presence of two karyotypes described from Itaquera (São Paulo) by
Studies on sexual compatibility, acoustic communication, chemical analyses of pheromones and cuticular hydrocarbons are, to some extent, complementary, as the Brazilian populations of the A. sp.1 morph used in these studies were the same. Specifically, A. sp.1 presented by Bento Gonçalves (Rio Grande do Sul), Vacaria (Rio Grande do Sul), São Joaquim (Santa Catarina) and Piracicaba (São Paulo) populations, revealed significant (P < 0.01) differences in the male pheromone composition (
Together, all the evidence reviewed on three Brazilian entities regarding visual incompatibility, acoustic communication and chemical profiles suggest that the combination of all three types of signals will be necessary for the development of an effective pest monitoring and management program since these studies pointed out that (i) sexual specificity in the production and perception of individual pheromone components in this species might exist (ii) synthetic mixture of the A. fraterculus male-borne pheromone was effective in attraction of conspecific females, suggesting the use of this mixture for the control of this pest in infested orchards (
Future studies focused on electrophysiological and behavioral studies of the chemical communication of Af complex could help to understand the complex relationships between the three Brazilian entities. Research on mating behavioral sequences of the three Brazilian entities of the Af complex as well as basic knowledge about A. fraterculus sexual communication could help to unravel mate assessment and mate choice dynamics, leading to the development of behavior-based control strategies and novel control tools for integrated pest management programs (
From an applied perspective, area-wide integrated pest management programs based on the Sterile Insect Technique (SIT) cannot use only one A. fraterculus population to cover all Brazil. However, one population may be used in SIT programs covering wide areas that share the same morphotype, male courtship behavior and same time of the day when matings occur (
The authors acknowledge Dr. Tara Massad for the language corrections and valuable comments, and Dr. Denise Selivon, Dr. Giovanni Benelli and the anonymous reviewer for their comments on the submitted version of the manuscript. Funding for this research was provided by the International Atomic Energy Agency (FAO, Austria, Vienna), through “Coordinated Research Project on Resolution of Cryptic Species Complexes of Tephritid Pests to Overcome Constraints to SIT and International Trade” (Research Contract Nos. 16106, 16965, 16051, 16080, and 16060).