Importance and evolution of sexual dimorphism in different families of Collembola ( Hexapoda )

A bibliographic revision of sexual dimorphism in different families of Collembola was performed in order to determine the most common patterns in each group. We list several examples of the sexual dimorphism in different families of Collembola, which illustrate from some of the smallest differences between males and females to major differences between both sexes in some families. We show different cases of sexual dimorphism in Spinactaletes, Sminthurides, and the remarkable morphology of Guthriella muskegis. It seems that most of the cases of strong sexual dimorphism are related to aquatic habitats or behaviour still not fully understood. Species belonging to primarily aquatic families (fresh water or marine water) have the most evolved morphology, where males have clasping antennae to attach the females in order to avoid loosing them with the movement of the water.


Introduction
Guaranteeing the transference of genetic information to subsequent generations is a fundamental task in all living beings.The success of this process is related to differences in the access to mating, or sexual selection (Darwin, 1871).On mating, competition appears generally between males to be selected by females.The sexual dimorphism in males of Hexapoda appears in different groups, showing complex patterns that include particular behavior for mating.
Nevertheless, even in groups in which there is no copulation, in which the males do not have much contact with females, and the transfer of sperm is done by other mechanisms, there is still some kind of sexual dimorphism.

Sexual dimorphism in Collembola families
According to the literature reviewed, there are sexual dimorphism records in ten of the 33 families of Collembola.Secondary sexual characters have been recorded in 28 genera.The main examples of sexual dimorphism, found in different families of Collembola, are shown in Table 1.
In the Symphypleona, sexual dimorphism is more evident, and this character affects head and antennae and the success of spermatophore transfer to the females, regardless of the environment (these modifications occur in edaphic habitats, as well as in aquatic, freshwater or marine littoral).In the case of the terrestrial Pseudachorutes (Neanuridae), two ventral organs were observed in the male (Gao & Palacios-Vargas, 2008), and interpreted as sexual dimorphism, which is very clearly symmetrical for both sides of the body.This kind of sexual dimorphism has been observed in other members of the Poduromorpha (as Onychiuridae), and might be common in other families.
In the case of the Isotomidae, the most extraordinary modifications in Guthriella muskegis are in the end of the body, in particular the presence of spines and modifications of the setae.Males present ornamentation similar to the patterns found in other groups of Arthropoda, as the Insecta, in order to attract females.These characteristics may only emerge when males are in the reproductive condition and males very similar to females can be found, even in the adult phase, without modifications.In modified males, the setae look like leaves and they develop abdominal spines, which are not present in the females; even the antennae are modified (Figure 1).There are also records of modifications of the antennae in other species of Isotomidae, their function are still unknown.The specimens of G. muskegis are from Cerro Fábrega, Bocas del Toro, Panama.
For the Entomobryidae, the main sexual differences are in the color patterns, and in the modification of mucro and genital aperture.
In the case of the species members of the littoral, Spinactaletes spp.(Spinactaletidae), the modifications are the presence of a spur in the tibiotarsus III and also clasping antennae in the males.
For the peculiar case of Coenaletes caribaeus Bellinger (Coenaletidae), which lives between the shell and the hermit crab, we studied the differences of males and females (Palacios-Vargas et al., 2000).The modifications include the presence of clasping antennae with spines and also some spines on thorax and abdomen, although their function are still unknown.

Conclusions
1.The habitat can be a very important factor determining the presence of several sexual characters.
2. Fresh water and marine littoral springtails present more important morphological modifications to facilitate sperm transfer from the male to the female.
3. In terrestrial species, the most extraordinary case is that of G. muskegis which ornamentation is similar to the patterns found in other groups of Arthropoda.

Figure 1 .
Figure 1.Female and male of Guthriella muskegis.Dorsal view of female (A), dorsal view of male (B), last abdominal segments in female (C), and last abdominal segments in male (D).