Specific Mate Recognition System Research Articles

In memory of Judith Masters and Fabien Génin.

In memory of Judith Masters and Fabien Génin.

Molecular evidence for introgressive hybridization in New Zealand masked gulls

We used mitochondrial DNA (mtDNA) gene sequences and nuclear microsatellite loci to investigate the extent and outcome of hybridization between the Black‐billed Gull Chroicocephalus bulleri and the Red‐billed Gull Chroicocephalus novaehollandiae scopulinus in New Zealand. Six of 26 sampled Black‐billed Gulls possessed mtDNA typical of Red‐billed Gulls, but allele frequencies at six polymorphic microsatellites provided little evidence of mixed ancestry expected in very recent hybrids. None of the Red‐billed Gulls sampled from different colonies possessed Black‐billed Gull mtDNA expected in the reciprocal cross, suggesting that hybridization in the two species typically occurs between female Red‐billed Gulls and Black‐billed Gull males. The lack of any hybrid signal in the nuclear loci indicates that there has been extensive backcrossing with Black‐billed Gulls, effectively diluting the Red‐billed Gull nuclear DNA contribution. Divergence of Red‐billed Gulls and Black‐billed Gulls occurred approximately 250 000 years ago, indicating that unsorted ancestral polymorphism is an unlikely alternative to hybridization. Comparing demographic models within an approximate Bayesian computation (ABC) framework, we confirm that the observed patterns cannot result from incomplete lineage sorting. Using an ABC random forest approach, we determined that the most likely model explaining the data is a recent introgression scenario, whereby unidirectional gene flow is re‐established following a period of strict isolation. The ability of Black‐billed and Red‐billed Gulls to successfully interbreed shows that despite significant differentiation (FST > 0.3), there has been insufficient time for the two species to develop complete reproductive isolation. The apparent one‐way transfer of Red‐billed Gull mtDNA into Black‐billed Gulls and extensive backcrossing argues against cytoplasmic–nuclear genome incompatibilities between the two species. We hypothesize that the specific mate recognition system cued on colours of soft parts normally functions to prevent hybridization, but that it can break down under demographic conditions where there is a shortage of available mates and a surplus of females in the Red‐billed Gull population. The high incidence of introgression in Black‐billed Gulls conflicts with field observations that interbreeding is extremely rare.

No pre-zygotic isolation mechanisms between Schistosoma haematobium and Schistosoma bovis parasites: From mating interactions to differential gene expression.

Species usually develop reproductive isolation mechanisms allowing them to avoid interbreeding. These preventive barriers can act before reproduction, "pre-zygotic barriers", or after reproduction, "post-zygotic barriers". Pre-zygotic barriers prevent unfavourable mating, while post-zygotic barriers determine the viability and selective success of the hybrid offspring. Hybridization in parasites and the underlying reproductive isolation mechanisms maintaining their genetic integrity have been overlooked. Using an integrated approach this work aims to quantify the relative importance of pre-zygotic barriers in Schistosoma haematobium x S. bovis crosses. These two co-endemic species cause schistosomiasis, one of the major debilitating parasitic diseases worldwide, and can hybridize naturally. Using mate choice experiments we first tested if a specific mate recognition system exists between both species. Second, using RNA-sequencing we analysed differential gene expression between homo- and hetero-specific pairing in male and female adult parasites. We show that homo- and hetero-specific pairing occurs randomly between these two species, and few genes in both sexes are affected by hetero-specific pairing. This suggests that i) mate choice is not a reproductive isolating factor, and that ii) no pre-zygotic barrier except spatial isolation "by the final vertebrate host" seems to limit interbreeding between these two species. Interestingly, among the few genes affected by the pairing status of the worms, some can be related to pathways affected during male and female interactions and may also present interesting candidates for species isolation mechanisms and hybridization in schistosome parasites.

The recognition concept and genetic approaches to interpreting species.

1. Introduction. 2. The Specific-mate Recognition System (SMRS). 3. The Genetic Change As sociated with Speciation.

Mate recognition systems and species limits in a warbling-finch complex (Poospiza nigrorufa/whitii)

ABSTRACTSpecies limits in the Poospiza nigrorufa/whitii complex are not well understood. Three taxa formally described as species are now considered as subspecies (nigrorufa, whitii and wagneri) of a widespread species. The heavier nigrorufa has longer bill, tarsus and wings, is slightly dimorphic with males showing tawny rufous throat, breast and flanks, and brownish grey upper parts with a slate tinge, while females differ in the orange tinge of ventral parts and in the more olivaceous upper parts; inhabits shrubby open areas and wetlands with reeds and bulrushes in eastern southern South America, and gives a simple three-note pattern that repeats to form the song and diagnostic calls. The lighter whitii (including wagneri as a synonym) has a shorter bill, tarsus and wings, is highly dimorphic with males having dark chestnut throat, breast and flanks, and slate upper parts, while females exhibit tawny pale-orange ventral parts, and olivaceous light-brown upper parts; inhabits closed to semi-closed xerophytic to semi-humid scrub and woodlands in the western highlands, and has a complex multi-noted song and diagnostic calls. Reciprocal playback experiments indicate that both taxa are able to discriminate each other’s songs. Locality data and ecological niche modelling show that nigrorufa and whitii are narrowly allopatric or parapatric in central Córdoba province (Argentina).This integrative evidence and the ~2.5% divergence in mtDNA show that nigrorufa and whitii possess different Specific Mate Recognition Systems and should be afforded full species status under any species concept.

Acoustic signals in insects: A reproductive barrier and a taxonomic character

In singing insects, the song is an important component of the specific mate recognition system (SMRS). In communities of sympatric singing species, there is a partitioning of communication channels, the so-called “acoustic niches.” Within one community, the songs of different species always differ in temporal or frequency characters, i.e. occupy different acoustic niches. However, conspecific songs do not always act as an interspecific reproductive barrier, despite always being a SMRS component. The species that do not communicate acoustically due to allopatry, different timing of vocalization, inhabiting different biotopes, or unmatched food specializations can produce similar songs while forming reproductively isolated communities. Individuals of different sexes need not only to recognize a conspecific mate but also to evaluate its “quality.” The close-range signal (courtship song) provides more opportunities for choosing the “best” male than does the distant signal (calling song). In many species of Orthoptera, courtship includes not only acoustic but also vibrational, visual, chemical, and mechanical signals. An analysis of cricket songs showed the courtship songs to be on average more elaborate and variable than the calling songs. At the same time, due to the difference in mating behavior between the two groups, the acoustic component of courtship is used for mate quality evaluation to a greater extent in grasshoppers than in crickets. The courtship songs of grasshoppers are generally more elaborate in temporal structure than cricket songs; moreover, they may be accompanied by visual displays such as movements of various body parts. Thus, song evolution in grasshoppers is more strongly driven by sexual selection than that in crickets. According to the reinforcement hypothesis, the premating barrier between hybridizing species becomes stronger in response to reduced hybrid fitness. However, our behavioral experiments with two groups of hybridizing grasshopper species did not confirm the reinforcement hypothesis. We explain this, firstly, by a low level of genetic incompatibility between the hybridizing species and secondly, by high hybrid fitness when attracting a mate. A high competitive capability of hybrids may be accounted for by attractiveness of new elements in hybrid courtship songs. When we divide similar forms based on their songs, we in fact distinguish biological species using the criterion of their reproductive isolation. Acoustic differences between species are usually greater than morphological ones. Therefore, song analysis allows one to determine the real status of doubtful species-rank taxa, to distinguish species in a medley of sibling forms, and to reveal cryptic species in the cases when morphological studies fail to provide a univocal result. At the same time, songs are subject to intraspecific variation the range of which is different in different groups. Therefore, it is necessary to study which degree of difference corresponds to the species level before interpreting the status of some forms based on song comparisons. Besides, song similarities cannot indicate conspecificity of acoustically isolated forms; on the other hand, song differences between these forms prove that they are full-rank species.

Mate Recognition in the South African Citrus Thrips Scirtothrips aurantii (Faure) and Cross-Mating Tests with Populations from Australia and South Africa

South African citrus thrips (Scirtothrips aurantii) is a pest of citrus, mango and other horticultural species in its native range, which encompasses a large part of Africa. Its adventitious establishment in Australia in 2002 was a major cause for concern. The thrips, 11 years after its incursion into Australia, has remained on plants of a single host plant genus Bryophyllum (Crassulaceae). Characterization of the Specific-Mate Recognition System of the Bryophyllum population of thrips present in Australia and behavioral bioassay experiments revealed that compounds found in the insects' body extracts play a crucial role in mate recognition of S. aurantii. Reciprocal cross-mating experiments between the Australian Bryophyllum insects and South African S. aurantii from horticultural host plants showed that mating frequencies were significantly lower in test crosses (Bryophyllum x horticultural) than in controls (Bryophyllum x Bryophyllum or horticultural x horticultural), which indicates there are at least two distinct species within S. aurantii and suggests further tests of this interpretation. The results suggest that these tiny phytophagous insects localize mates through their association with a particular host plant species (or closely-related group of species). Also, specific tests are suggested for clarifying the species status of the host-associated populations of S. aurantii in Africa.

Copulatory Courtship Behavior and Sine Song as a Mate Recognition Cue inDrosophila liniand Its Sibling Species

Most Drosophila species sing species-specific pulse songs during their "precopulatory courtship." Three sibling species of the Drosophila montium species subgroup performed "copulatory courtship": males generated courtship songs by vibrating either wing only after mounting and during copulation. In these three species, strong sexual isolation was detected between D. ohnishii and D. lini and between D. ohnishii and D. ogumai, but not between D. lini and D. ogumai. Female showed strong repelling behavior when they were mounted by a heterospecific male in the species combinations including D. ohnishii, resulting in failure of the copulation attempt of the male. Acoustic analyses of courtship songs revealed that the pulse song was irregular, without any species-specific parameters, but that the frequency of the sine song was different among the three species in accordance with the modes of sexual isolation between them; it was significantly lower in D. ohnishii (mean ± SE = 193.0 ± 1.7 Hz) but higher in D. lini (253.4 ± 2.7 Hz) and D. ogumai (246.7 ± 5.3 Hz). We suggest that this difference in the sine song frequency is a sexual signal in the Specific Mate Recognition System (SMRS) among these three Drosophila species.

Relative Effects of Juvenile and Adult Environmental Factors on Mate Attraction and Recognition in the Cricket,Allonemobius socius

Finding a mate is a fundamental aspect of sexual reproduction. To this end, specific-mate recognition systems (SMRS) have evolved that facilitate copulation between producers of the mating signal and their opposite-sex responders. Environmental variation, however, may compromise the efficiency with which SMRS operate. In this study, the degree to which seasonal climate experienced during juvenile and adult life-cycle stages affects the SMRS of a cricket, Allonemobius socius (Scudder) (Orthoptera: Gryllidae) was assessed. Results from two-choice behavioral trials suggest that adult ambient temperature, along with population and family origins, mediate variation in male mating call, and to a lesser extent directional response of females for those calls. Restricted maximum-likelihood estimates of heritability for male mating call components and for female response to mating call appeared statistically nonsignificant. However, appreciable “maternal genetic effects” suggest that maternal egg provisioning and other indirect maternal determinants of the embryonic environment significantly contributed to variation in male mating call and female response to mating calls. Thus, environmental factors can generate substantial variation in A. socius mating call, and, more importantly, their marginal effect on female responses to either fast-chirp or long-chirp mating calls suggest negative fitness consequences to males producing alternative types of calls. Future studies of sexual selection and SMRS evolution, particularly those focused on hybrid zone dynamics, should take explicit account of the loose concordance between signal producers and responders suggested by the current findings.

Pheromone communication channels in tortricid moths: lower specificity of alcohol vs. acetate geometric isomer blends

Discrimination of conspecific and heterospecific signals is a key element in the evolution of specific mate recognition systems. Lepidopteran pheromone signals are typically composed of several compounds that synergize attraction of conspecific and inhibit attraction of heterospecific males. Blends convey specificity, but not their single components, that are typically shared by several species. Many sex pheromones are blends of geometric or positional isomers of straight-chain acetates, while species-specific blends of analogous alcohols have not been described. We have, therefore, studied the attraction of tortricid moths to the geometric isomers (E,E)-, (E,Z)-, (Z,E)- and (Z,Z)-8,10-dodecadien-1-ol. Only one species responding to these alcohols seemed to be attracted to a blend of two isomers, while most species are attracted to only one alcohol isomer. Lack of a pronounced synergist or antagonist effect of the other geometric isomers explains the lack of specific attraction to isomer blends and reduces accordingly the number of specific communication signals composed of these alcohols. In comparison, many more species respond to the analogous (E,E)-, (E,Z)-, (Z,E)- and (Z,Z)-8,10-dodecadienyl acetates and their binary blends. The acetate isomers all play a behavioural role, either as attractants, attraction synergists or antagonists, and thus promote specific communication with acetate blends. Male moths seem to discriminate the acetate isomers with greater precision than the analogous alcohols. It is proposed that discrimination is facilitated by steric differences between the four acetate isomers, as compared to the more uniform steric properties of the alcohols.

Mitochondrial DNA variation and the evolutionary history of the Mediterranean species ofCicadaL. (Hemiptera, Cicadoidea)

Cicadas are widely distributed in the Mediterranean area and are mainly distinguished by male acoustic signals, which act as specific mate recognition systems. Within the genus Cicada L. several species have diverged in their calling songs without showing external morphological differences, so acoustic recordings and genetic studies are particularly useful for systematic, biogeography and evolutionary studies. This study assesses sequence variation in closely related species of Cicada from the Mediterranean area, using domain III of the 12S rRNA mitochondrial gene in order to determine the phylogenetic relationships and the evolutionary history of this group, as well as the population structure of the two most common species, C. orni and C. barbara. Five distinct haplogroups were identified, C. orni, C. barbara, C. mordoganensis, C. cretensis and C. lodosi, each corresponding to a distinct evolutionary group. C. barbara was the most divergent species within this group, while C. orni and C. mordoganensis were the most similar. The population structure and demographic parameters of the species were not completely resolved. However, there is evidence for the separation of the C. orni Greek populations from the rest of Europe and also for demographic expansions probably related to Pleistocene climate changes. © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 155, 266–288.

Calling songs of sympatric and allopatric populations of Cicada barbara and C. orni (Hemiptera: Cicadidae) on the Iberian Peninsula

Calling songs of the sibling species Cicada barbara and C. orni were studied in sympatric and allopatric populations on the Iberian Peninsula, where the distribution ranges of both species overlap. No difference was found in any acoustic property for the sympatric and allopatric populations of C. barbara studied and only one variable (minimum frequency) was significantly different between sympatric and allopatric populations of C. orni. No hybrids with intermediate songs were found and no character displacement in the calling song was detected. It is very likely that these species were already considerably differentiated when they met on the Iberian Peninsula. Particularly, premating (or even postmating) isolating mechanisms (according to Mayr's Biological Species Concept) or different specific-mate recognition systems (in the view of the Paterson's Recognition Concept of Species) were most likely already present, which prevented hybridization between this pair of species. It is assumed that the calling songs are the most important premating isolating mechanism corresponding to the specific-mate recognition systems of these species of cicadas.

Visual Communication Behaviour as a Mechanism Behind Reproductive Interference in Three Pygmy Grasshoppers (Genus Tetrix, Tetrigidae, Orthoptera)

Specific mate recognition systems should enable species to recognize conspecific mates correctly. However, heterospecific matings have been observed in a variety of taxa. One of these cases is the pygmy grasshopper genus Tetrix, in which three species show sexual interactions. T. ceperoi males mount preferably females of T. subulata, but they are rejected as mates. T. subulata males prefer T. undulata females over conspecific females and heterospecific matings occur. Here, we study the underlying behavioural mechanisms of this pattern by analysing the visual courtship behaviour of the three species videographically. We test the hypothesis that the displays of T. ceperoi are highly differentiated from the other species, while the courtship of T. subulata and T. undulata is more similar. This is supported by our results: while T. ceperoi males perform a fast movement of high amplitude (“pronotal bobbing”), the other two species show only minor movements (“lateral swinging,” “frontal swinging”). The first function of a discriminant analysis of the temporal dimensions of the displays explained 96% of the variance. 100% of the T. ceperoi displays were classified correctly, whereas only 50% of the T. subulata and 81% of the T. undulata displays were grouped accurately. A two-way ANOVA revealed no significant effects of the direction of the “swinging” movements (laterally or frontally) and no interactions between direction and species either, whereas each temporal parameter differed significantly between the three species. The highest degree of differentiation was found between T. ceperoi and T. undulata, while T. subulata and T. undulata only differed significantly in two of the six temporal parameters. Our results suggest that the mismatings between T. undulata and T. subulata are caused by an insufficient specificity of the courtship behaviour. Apparently, ecological segregation of these two species could impede sexual interactions in the field.

Chemical constraints on the evolution of olfactory communication channels of moths

It is estimated there are over 100,000 moth species (Lepidoptera) that produce sex pheromones comprising communication channels used in specific-mate-recognition systems (SMRS) involved in pre-zygotic mating isolation and speciation. About 1572 moth species have been found to use 377 pheromone components, the majority being alcohols, aldehydes or acetate esters of olefinic chains of 10–22 carbons. Since there are limited numbers of possible unsaturated (double bonded) E- and Z-configured isomers of these chains, there may be constraints on incipient species evolving new pheromone components, especially if they are utilized by existing species. Here I develop algorithms that count and name all possible structures of chains with or without a functional group. The results show that for acetate esters there are only seven or nine monounsaturated isomers of six or seven carbon chains, respectively, suggesting use of these compounds could limit the number of communication channels available for radiation of new species (no moths use these short chains). For commonly used 14-carbon chains with an acetate ester functional group, and 1–3 unsaturations, there are 1039 isomers. A total of 2,096,883 isomers were counted from all multiply unsaturated 10–22-carbon chain acetate esters. The number of possible signals quickly extends into millions when considering pheromone blends of 2–4 components used by most species. There should be little chemical constraint on evolution of new communication channels based on compounds of 10 or more carbons, even for closely related species (e.g. ermine moths, Yponomeuta).

Vibrational communication in insects

Communication through substrate-borne vibrations has for long been recognized but in comparison with air-borne sound it has received very little attention. However, in recent years it has become increasingly clear that vibrational signals play a crucial role in communication in many insect groups and we provide a short overview. Vibrational signals are related to sexual behavior, alarm and defensive behavior and are often used to mediate coordinated group actions and complex social interactions. For small insects they are probably the least costly and most far-reaching signals for intraspecific communication and also not easily perceived by a potential predator or parasitoid. Substrate-borne signals are produced by diversed methods and detected by sensitive receptors in all six legs. The courtship behavior of the southern green stink bug Nezara viridula (L.) (Hemiptera: Pentatomidae) is taken as a representative model in illustrating some principal mechanisms of vibrational communication in insects. Species and sex specific vibrational signals produced during the courtship are well suited for propagation through plants and to transmit the relevant information about the species and sex of the sender as well as provide the directional cue for locating the mate. The role of substrate-borne signals as a part of the specific mate recognition systems which are unique for each species makes studies of vibrational signals a very useful tool for resolving taxonomic problems.

Three acoustic forms of Allen's galagos (primates; Galagonidae) in the Central African region.

This study identifies populations currently classified as Allen's galago (Galago alleni) at ten locations in Gabon, Cameroon and Bioko Island. Morphological diversity was evident both within and between populations. Attention to the loud calls revealed three distinct vocal profiles which are consistent within biogeographical regions. This work is based on the Recognition Concept of Species which refers to a Specific Mate Recognition System. Galagos rely less on visual signals than diurnal primates and recognise each other principally by means of auditory and olfactory signals. Galagos possess repertoires of loud calls relating to contact and alarm which are thought to be species-specific. Other studies of nocturnal prosimians (galagos, tarsiers) have demonstrated that the unique loud call repertoires are reliable indicators of species boundaries; whereas characters such as body size and pelage coloration are highly variable, even within populations. The vocal data in this study provide evidence of at least three acoustic forms of galago within the Allen's group which are predicted to represent three distinct species: the Allen's form on Bioko Island and south-west Cameroon, the Gabon form in southern Cameroon and northern Gabon and the Makandé form in Gabon south of the Ogooué river. Some populations may be vulnerable to extinction due to limited distributions and habitat destruction.

Variations in call and morphology in male water frogs: taxonomic and evolutionary implications

In Anurans, the specific mate recognition system (SMRS), which contributes to prezygotic isolation, is mainly based on morphological and call features. This is why such criteria are used by zoologists for taxonomic identification. In hybridogenetic water frogs ( Rana ridibunda, R. lessonae, R. perezi, R. kl. grafi and R. kl. esculenta), hybridization opens up the question of the efficiency of these criteria for taxon identification and of the specific recognition system in this context. Variation in both morphological and call features revealed both significant mean differences among taxa but also large overlapping among individuals belonging to different taxa. Thus, using call or morphometrical features in order to identify water frogs may be hazardous. Moreover, species differ poorly in their specific mate recognition system, facilitating hybridization events, and therefore suggesting that postzygotic mechanisms may be prevalent over prezygotic mechanisms.

A new subspecies of the Red-billed Hornbill, Tockus erythrorhynchus, from West Africa

Trea, B. & Erord, C. 2000. A new subspecies of the Red-billed Hornbill, Tockus erythrorhynchus, from West Africa. Ostrich 71 (3&4):363-366.The Red-billed Hornbill, Tockus erythrorhynchus (Temminck), over most of its distribution range, has pale yellow or pink facial skin. However, in Senegal, The Gambia and Western Mali, where all Red-billed Hornbills are usually referred to the nominate subspecies, all adults have black circumorbital (facial) bare skin, conspicuous on live birds as well as on skinned specimens, and brown eyes. Field and museum studies suggest that these black-faced and brown-eyed birds from the western-most part of Africa belong to a yet undescribed subspecies. A review of the documents (including various black-and-white ond colour plates) on which Temrninck based his original description and naming of the species shows that there is uncertainty obout the locality of the type specimen illus-trated in the originol description. Furthermore, neither the plates nor their accompanying texts show the black facial pattern charac-teristic of these westem-most West African populations. To avoid confusion in future, and to ensure nomenclatural stability, a new type-locality and a neotype are designated for nominate Tockus erythrorhynchus, and a new nome is proposed for the populations extending from Senegal, The Gambia and Guinea to the inner Niger Delto in Mali. Further studies are needed to ascertain the status of these brown-eyed and black-faced birds: their facial colouration pattern could be associated with other eco-ethological characters and could play an important role in specific mate recognition sys-tems. [A French translation of the abstractis provided on p. 366.]

Is the spinule pattern on the leg 4 coxopodite a tactile signal in the specific mate recognition system of Mesocyclops (Copepoda, Cyclopidae)?

Several recent observations on e.g. birds and fruit flies support the hypothesis that when previously geographically separated populations, as neospecies, come into contact, sexual isolation mechanisms become stronger as a result of direct selection against inferior hybrids (reinforcement hypothesis). Many aspects of the reproductive biology of cyclopid copepods are still very poorly known. However, all reports on mating processes in the genus Mesocyclops confirm that males attach to the fourth legs of the females by their geniculate antennulae before transferring spermatophores. Accordingly, it is reasonable to assume that the signals helping recognition of the conspecific mates are located on the leg 4 of the females. The posterior surface of the leg 4 coxopodite in Cyclopidae is ornamented with a complex and diverse spinule pattern which, despite some infraspecific variability, is a reliable species-specific trait in species of Mesocyclops. Depending upon whether the spinule ornamentation has any role in the recognition system, and whether it evolved in geographically separated populations or later when they had begun to overlap, different predictions can be made about the zoogeographical pattern of differences among these character states. In the following study, comparisons are made for 10 allopatric, four sympatric and two partially sympatric species pairs. These comparisons reveal that the degree of divergence in the spinule ornamentation is significantly greater between sympatric than between allopatric species. These results argue in favor of the spinule ornamentation of the leg 4 coxopodite being a signal in specific mate recognition system (SMRS), and that the divergence of this state is initiated when previously separated populations, as neospecies, begin secondary contact.

Female leg 4 development in Laophontidae (Harpacticoida): a juvenile adaptation to precopulatory behaviour

Development of postmaxillipedal appendages in harpacticoid copepods is in general identical in both sexes. Exceptions are minor and result merely in secondary sexually dimorphic structures of the endopodites. From the third copepodid stage on, females of several laophontid species develop an entirely different leg 4 exopodite than in males. Whereas the male leg has a normal morphology, the female leg appears as a large flattened and sturdily sclerified structure. This structure remains present until copepodid V but is drastically reshaped during the terminal moult resulting in a normally ornamented and segmented adult leg. Thus far, the family Laophontidae is the only harpacticoid taxon of which it is known that adult males clasp the 4th or 5th leg of subadult females during mate guarding. The curious shape of leg 4 in subadult females is considered as a juvenile adaptation of the original developmental pattern to facilitate clasping by the adult males. Within the family this juvenile adaptation evolved from a simple anchorage for the male antennulae to a highly advanced morphological complex indicating that it functions as a specific mate recognition system (SMRS).