The caudal bursa in the Heligmonellidae (Nematoda: Trichostrongylina). Characterization and hypothesis on its evolution

The different patterns of the caudal bursa of the Heligmonellidae (Nematoda) are redefined, taking into account the grouping of rays 2-6 and the sequence of origin of these rays from their common trunk. The type of symmetry of the caudal bursa is also redefined. The following patterns were observed and characterized: the basic patterns: types 2-3, 2-2-1, 1-3-1 and 1-4 and the intermediary patterns: type 2-3 tending to type 2-2-1, type 2-2-1 tending to type 1-3-1, type 1-3-1 tending to type 1-4 and type 2-2-1 tending to type 1-4. An evolutionary interpretation of the patterns is attempted and seems to follow the direction: 2-3 to 2-2-1 to 1-3-1 to 1-4. Seven atypical patterns are described. The caudal bursae were classified based on their symmetry: subsymmetrical, dissymmetrical and asymmetrical. Independently of the type of symmetry, the two latero-ventral lobes may have the same or different patterns. The type of symmetry, the ratio between the two latero-ventral lobes and a characteristic pattern were utilized to characterize the caudal bursae at the level of the genus and the subfamily. The combination of the right/left ratio and the type of symmetry gives heterogeneous results, with no real association between these characters. The most conspicuous asymmetries and dissymmetries were found among the Nippostrongylinae. The most frequent pattern in the Heligmonellidae is the basic type 2-2-1; types 1-3-1 and 1-4 are less frequent but are characteristic of several genera; type 1-4 is absent from the Heligmonellinae. Whatever the pattern, in the Heligmonellidae rays 4 and 5 are the last to diverge from the common trunk of rays 2-6.


T he Trichostrongylina have a common origin
with the other suborders of the order Strongylida, arising from an ancestor close to the Rhabditida (Durette-Desset et al., 1994;Blaxter et al., 1998Blaxter et al., , 2001. In the strongylid nematodes, unlike the Rhabditida, the tail of the male widens in order to form a caudal bursa made up of two latero-ventral lobes and one dorsal lobe. Therefore the caudal bursa is a derived character regarded as a synpomorphy for the Strongylida. Durette-Desset & Chabaud (1981) and Durette-Desset (1985), proposed a classification of the Trichostrongyloidea which they divided into three supra familiar groups: the "Trichostrongylids", the "Molineids" and the "Heligmosomids". In these classifications, they highlighted various types of caudal bursae, based mainly on the grouping of rays 2 to 6 (i.e. the rays supporting the latero-ventral lobes) (Fig.  1). In 1981, four patterns were defined: 1-3-1, characteristic of the "Trichostrongylids", 2-1-2, characteristic of the "Molineids" and 2-2-1 and 3-2, characteristic of the "Heligmosomids". Durette-Desset (1985) added type 2-3 and specified that each grouping is characteristic of a given evolutionary line or a given family. Then, Durette-Desset & Chabaud (1993) raised the Trichostrongyloidea to a suborder: the Trichostrongylina and each supra familiar group became a superfamily: the Trichostrongyloidea, the Molineoidea and the Heligmosomoidea.
This descriptive system however seems to us to be insufficient to properly describe the caudal bursae of some Nippostrongylinae, especially the genera such as Heligmonina Baylis, 1928 andStilestrongylus Freitas, Lent &Almeida, 1937, which do not show the same pattern in each lateral lobe. Within the framework of a revision of the Heligmonellidae, the aim of this work is to redefine the different patterns of the caudal bursa found within this family, taking into account not only the grouping of rays 2-6 but also the sequence of origin of these rays from their common trunk. The type of symmetry of the caudal bursa is also redefined. This enables us not only to make the descriptions of the caudal bursae more accurate, but also to highlight the characteristic type(s) of pattern within each genus and to attempt an evolutionary interpretation of the patterns.

MATERIALS AND METHODS
T he elements usually considered in the description of a caudal bursa (CB) are: symmetry, pattern of latero-ventral lobes, development of the dorsal lobe and characters of the dorsal ray and rays 8. The characters of the dorsal ray and rays 8 are not treated in this work. Some terms concerning the symmetry and the pattern of the latero-ventral lobes are redefined as follows.

TYPES OF SYMMETRY
There are three types, which concern the degree of development of the latero-ventral lobes in relation to the sagittal axis of the worm: -Subsymmetrical bursae (CB SS): both lobes are of similar size and shape in relation to the axis of the dorsal ray, which passes through the sagittal axis of the worm (Fig. 2a).
-Dissymmetrical bursae (CB DS): One lobe is larger than the other in relation to the axis of the dorsal ray, which passes through the sagittal axis of the worm. When the right lobe (RL) is larger it is cited as CB DS RL+. When the left lobe (LL) is larger it is cited as CB DS LL+ (Fig. 2b).
-Asymmetrical bursae (CB AS): The axis of the dorsal ray does not pass through the sagittal axis but is displaced to the right or the left side of the worm. One lobe may or may not be larger than the other in relation to this axis. When the right lobe (RL) is larger it is cited as CB AS RL+. When the left lobe (LL) is larger it is cited as CB AS LL+ (Fig. 2c).

LITERATURE DATA
The data were compiled from descriptions published in the literature. We took into account only the caudal bursae where both latero-ventral lobes, or at least one, was spread out. In the latter case, the lobe was treated separately and the pattern was not extrapolated to the entire bursa.  The systematic position of some species remains uncertain since, even if the caudal bursa is completely described, this is not the case with the synlophe. These species have therefore not been considered in this work. They are as follows: Durettestrongylus travassosi (Lent & Freitas, 1938), Heligmonella vladimiri Sadovskaja, 1952, Heligmonina vogeli Khalil, 1931, Heligmonoides crassidorsualis Franco, 1967, Heligmonoides mirzai Smales, 2008, Heligmosomum delta Travassos, 1921, Longistriata degusi Babero & Cattan, 1975, Longistriata castrosilvai Almeida, 1934, Longistriata fortuita Freitas, Lent & Almeida, 1937, Longistriata perfida Travassos, 1943 a. Subsymmetrical: both lobes are of similar size and shape in relation to the axis of the dorsal ray, which passes through the sagittal axis of the worm. Ex: Pudica gamma (Travassos, 1918). After Travassos (1921), modified. b. Dissymmetrical: one lobe is better developed in relation to the axis of the dorsal ray, which passes through the sagittal axis of the worm. Ex: Malvinema scapteromys (Suriano & Navone, 1996). In this case, it involves the right lobe. After Digiani et al. (2003), modified. c. Asymmetrical: the axis of the dorsal ray does not pass through the sagittal axis but is displaced to the right or left side of the worm. Both lobes may or may not have the same degree of development with respect to the axis of the dorsal ray. Ex: Malvinema victoriae Digiani, Sutton & Durette-Desset (2003). In this case, the right lobe is slightly better developed. After Digiani et al. (2003), modified. The levels of divergence of rays 2 to 6 from the common trunk are indicated by the dotted lines, which are perpendicular to a main axis represented by a straight line passing through ray 4. Ex: Malvinema carolinae Digiani, Sutton & Durette-Desset (2003). In the right lobe, ray 2 is the first (the most proximal ray) to diverge from the common trunk; the point of divergence of ray 3 is distal to that of ray 6. Rays 4 and 5 are the last to diverge.

DESCRIPTION OF THE PATTERNS
• Basic and intermediary types . Type 2-3 ( Fig. 3a) -Rays 2 and 3 grouped, arising first and together from common trunk of rays 2 to 6. -Rays 2 and 3 grouped from base in V-shape.
e. Type 2-3 t 2-2-1. Rays 2 and 3 are grouped, arising first and together from the common trunk of rays 2 to 6; rays 4 to 6 have a common trunk; ray 6 diverges close to the level of the divergence of ray 3 and proximally to that of rays 4 and 5. Ex: Neoheligmonella acomysi Durette-Desset & Gibson, 1990. In this case rays 2 and 3 are apposed for much of their length. After Durette-Desset & Gibson (1990), modified. f. Type 2-2-1 t 1-3-1. Rays 2 and 6 arise first and at the same level from the common trunk of rays 2 to 6; rays 3 arise just distally to the level of divergence of rays 2 and 6; rays 4 and 5 are the last to diverge. Ex: Pudica pudica (Travassos, 1921). After Cassone & Durette-Desset (1991), modified. g. Type 1-3-1 t 1-4. Rays 2 arise first from the common trunk of rays 2 to 6; rays 6 arise slightly distally to the level of divergence of rays 2 and proximally to that of rays 3; rays 3 to 6 have a short common trunk. Ex: Spalacina yanchevi . After Biserkov et al. (1995, modified. h. Type 2-2-1 t 1-4. Rays 2 arise first from the common trunk of rays 2 to 6; rays 3-6 have a short common trunk; rays 6 arise at the same level as rays 3; rays 4 and 5 are the last to diverge. Ex: Hypocristata anguillula (Durette-Desset, 1971). Ray 3 is still grouped with ray 2 since its extremity supports the ventral lobe. After Durette-Desset (1971), modified.
-Divergence of ray 6 proximal to divergence of rays 4 and 5 and approximately at same level of divergence of ray 3. . Type 2-2-1 (Fig. 3b) -Rays 2 and 3 grouped, arising first and together from common trunk of rays 2 to 6. -Ray 6 arising at the same level as ray 3.
-Rays 3 to 6 having short common trunk.
-Distal divergence of rays 4 and 5. Remarks In the patterns where rays 2 and 3 are grouped, the grouping shows different types: rays 2 and 3 may be joined to a lesser ( Fig. 3e) or greater extent ( Fig. 4a) or having a V-shape with the branches separated to a lesser ( Fig. 4b) or greater extent (Fig. 4c). In the latter case, rays 2 and 3 may be very distant from each other at their extremity, however both rays are all the same considered as grouped with rays 3 still supporting the ventral lobe. Such cases can be included in type 2-2-1 ( Fig. 4c) or 2-2-1 t 1-4 ( Fig. 3h), depending respectively on the presence or the absence of a short common trunk of rays 3 to 6. In type 1-3-1, on the common trunk of rays 3 to 5, ray 3 can diverge proximally to (Fig. 3c, RL), at same level as (Fig. 3c, LL), or distally to (Fig. 4d, RL) ray 5. In type 1-4, on the common trunk of rays 3 to 6, ray 3 can diverge proximally to (Fig. 3c, RL), at same level as (Fig. 3d, LL), or distally to (Fig. 4d, LL) ray 6.
• Atypical patterns Seven atypical patterns were found among the Heligmonellidae: Review e. Type 1-1-2-1. Rays 2 arise first from the common trunk of rays 2 to 6; rays 3 are completely separated and parallel to rays 2 and arise at the same level as rays 6; rays 4 and 5 are the last to diverge. Ex: left lobe of Cordicauda cordicauda (Durette-Desset, 1966). After Durette-Desset (1966), modified. f. Type 1-3-1 t 4-1. Ray 6 arises first from the common trunk of rays 2 to 6; ray 2 arises just distally to the level of divergence of ray 6 and rays 2 to 5 have a short common trunk. Ex: right lobe of Nippostrongylus magnus (Mawson, 1961). Type 4-1. Ray 6 arises first from the common trunk of rays 2 to 6 and rays 2 to 5 have a long common trunk. Ex: left lobe of N. magnus. After Beveridge & Durette-Desset (1992), modified. g. Type 3-1-1. Rays 5 and 6 arise first but separately from the common trunk of rays 2 to 6 and rays 2 to 4 have a long common trunk. Ex: left lobe of Nippostrongylus marhaeniae Hasegawa & Syafruddin, 1995. The right lobe shows a pattern of type 1-3-1 t 4-1. After Hasegawa & Syafruddin (1995), modified. h. Type 1-2-1-1. Ray 2 arises first from the common trunk of rays 2 to 6; rays 3 and 4 are grouped and rays 5 and 6 arise separately and at the same level as the group formed by rays 3 and 4. Ex: left lobe of Sciuricola moreli (Gibbons, Durette-Desset & Daynes, 1977). The right lobe shows a pattern of type 2-2-1. After Durette-Desset (1974), modified. i. Type 1-2-2. Ray 2 arises first from the common trunk of rays 2 to 6; rays 3 and 4 are grouped; rays 5 and 6 have a short common trunk and arise at the same level as ray 2 and the group formed by rays 3 and 4. Ex: right lobe of Trichoslinstowia maseri Durette-Desset & Vaucher, 1974. After Durette-Desset & Vaucher (1974, modified. Type 2-1-2. Rays 2 and 3 are grouped and arise first from the common trunk of rays 2 to 6; ray 4 is isolated; rays 5 and 6 have a short common trunk and arise at the same level as ray 4 and the group formed by rays 2 and 3. Ex: left lobe of T. maseri. After Durette-Desset & Vaucher (1974), modified.
-Rays 5 and 6 having short common trunk, arising at the same level as ray 2 and group formed by rays 3 and 4. . Type 2-1-2 ( Fig. 4i, LL) -Rays 2 and 3 grouped and arising first from common trunk of rays 2 to 6. -Ray 4 isolated.
-Rays 5 and 6 having short common trunk, arising at the same level as ray 4 and group formed by rays 2 and 3.

EVOLUTIONARY INTERPRETATION OF THE PATTERNS
Durette-Desset (1985) highlighted two evolutionary trends treating the Strongylida as a set: (1) reduction of the dorsal lobe (in the Rhabditida the tail of the male is vertically elongated) and (2) lengthening of rays 4, as papillae 4 of the Rhabditida are close to the anus (see Osche 1958;Chabaud et al., 1970 for the homology between the papillae of the Rhabditida and the bursal rays of the Strongylida) (Figs. 5a, 5b). Therefore Durette-Desset (1985) suggested that a caudal bursa with a short dorsal lobe and long rays 4 should be considered as highly evolved. Though these trends occur in each type of bursa, in general, types 2-1-2 and 2-3 (among the five types of pattern recognized) were considered as basal types for two reasons: they are the closest to the pattern of the Rhabditida with a well developed dorsal lobe and short rays 4; and they are also present in all four suborders of the Strongylida. However, no further attempt was made to explain the other patterns from an evolutionary point of view. We propose the following interpretation (Fig. 5c).
The transition from type 2-2-1 to type 1-3-1 involves a progressive migration of ray 3 towards ray 4 along with a progressive shortening of the dorsal lobe and ray 6, as observed in the intermediary type 2-2-1 t 1-3-1 (Fig. 3f). In type 1-3-1 (Fig. 3c), the migration of ray 3 towards rays 4 is achieved, with the appearance of a common trunk of rays 3-5, and ray 6 diverges from this common trunk at same level as ray 2.
The transition from type 1-3-1 to type 1-4 involves a distal migration of ray 6, with the appearance of a common trunk of rays 3 to 6, and a progressive lengthening of this trunk, as observed in the intermediary type 1-3-1 t 1-4 (Fig. 3g). In type 1-4 (Fig. 3d), only ray 2 arises first from the common trunk. This type of caudal bursa widens laterally and its width is greater than its length. The evolutionary steps then seem to follow the direction: 2-3 to 2-2-1 to 1-3-1 to 1-4, which is consistent with the early interpretation by Durette-Desset (1985) with respect to the basal patterns and the caudal bursae in which the width is greater than the length. Several descriptions of caudal bursae, especially in species of Heligmonina where the pattern was described as being of type 1-4 tending to type 1-3-1 (see for example Diouf et al., 2005) are therefore inaccurate from an evolutionary point of view. Some lobes may show a pattern of intermediary type 2-2-1 t 1-4 (Fig. 3h). This transition from type 2-2-1 involves the lengthening from the base of the set of rays 3-6 just after the divergence of ray 2, with the appearance of a short common trunk of rays 3 to 6 (intermediary type 2-2-1 t 1-4  , 1975 shows a type 1-4 in both lobes. We thus consider this type 2-3 as different from that of the most basal species. It may be derived from the type 1-4 by the migration of ray 3 towards ray 2, whereas rays 4 to 6 still have a long common trunk. • Atypical patterns . Type 1-1-2-1 (Fig. 4e) is present in the left lobe of Cordicauda cordicauda (Durette-Desset, 1966) (Brevistriatinae). This type seems to have been derived from type 2-2-1 by the isolation of ray 2 and short migration of ray 3 on the common trunk of rays 2 to 6. . Type 1-3-1 t 4-1 (Fig. 4f, RL) is present in the right lobes of Nippostrongylus magnus (Mawson, 1961) and N. marhaeniae Hasegawa & Syafruddin, 1995 (Nippostrongylinae). The transition from type 1-3-1 to type 4-1 involves a distal migration of ray 2 towards ray 3, forming a short common trunk of rays 2 to 5. Ray 6 is the most proximal ray to diverge from the common trunk of rays 2-6 and ray 2 arises just slightly distally to ray 6. . Type 4-1 (Fig. 4f, LL) is present in both lobes of Nippostrongylus sembeli Hasegawa & Tarore, 1995;and in the left lobes of N. magnus, N. rauschi Desset, 1966 andN. typicus (Mawson, 1961). This type seems directly derived from type 1-3-1, involving a marked distal migration of ray 2 towards ray 3. Ray 6 is the most proximal ray to diverge from the common trunk of rays 2-6, and rays 2 to 5 form a long common trunk on which ray 2 arises distinctly distally.
. Type 3-1-1 (Fig. 4g, LL) is present in the left lobes of four species of Nippostrongylus: N. djumachani (Tenora, 1969), N. marhaeniae, N. rysavyi (Erhardova, 1959 and N. witenbergi Greenberg, 1972. It seems directly derived from type 4-1 by the migration of ray 5 from its base towards ray 6. Ray 5 diverges from the common trunk at the same level as ray 6 and there is persistence of the common trunk of rays 2 to 4. . Type 1-2-1-1 (Fig. 4h, LL) is present in the left lobes of Sciuricola dremomys (Yen, 1973) and S. moreli (Gibbons, Durette-Desset & Daynes, 1977) (Heligmonellinae). It seems directly derived from type 1-3-1 by the migration (but not apposition) of ray 5 towards ray 6, with persistence of the group formed by rays 3 and 4. . Type 1-2-2 ( Fig. 4i, RL) is present in the right lobe of Tricholinstowia maseri Durette-Desset & Vaucher, 1974 (Heligmonellinae). It seems to be derived from type 1-3-1 (present in the other species of Tricholinstowia) by the migration of ray 5 towards ray 6. Type 2-1-2 ( Fig.  4i, LL) is present in the left lobe of the same species. It could be derived from type 1-2-2 by the migration of ray 3 towards ray 2, along with the absence of common trunk between rays 3 and 4. A pattern of type 2-1-2 is characteristic of the Molineoidea. However, type 2-1-2 of the Molineoidea is interpreted as a basal pattern, also characterized by short rays 4, whereas the pattern found in T. maseri, with long rays 4, is considered as derived from a 1-3-1 type. In this case, we consider the presence of this type in one lobe of Heligmonellidae as a convergence.

CRITERIA UTILIZED FOR THE CHARACTERIZATION OF THE CAUDAL BURSAE OF THE HELIGMONELLIDAE
• Type of symmetry (definition and examples above) At the specific level, a caudal bursa may be subsymmetrical (CB SS); dissymmetrical with right lobe larger (CB DS RL+); dissymmetrical with left lobe larger (CB DS LL+); asymmetrical (CB AS); asymmetrical with right lobe larger (CB AS RL+); asymmetrical with left lobe larger (CB AS LL+). At the generic level, we consider that a given genus may be characterized by the type of symmetry most frequently found among the species belonging to this genus.
• Evolutionary comparison between lobes As mentioned above, a species can have the same or a different pattern in both latero-ventral lobes. On the other hand, as seen above, the different patterns may be interpreted from an evolutionary point of view. This determines three types of "evolutionary ratio" between both lateral lobes ("right/left ratio") in a caudal bursa: (1) the same pattern in both lobes; (2) the pattern of the right lobe is derived with respect to that of the left lobe ("RL derived"); or (3) the pattern of the left lobe is derived with respect to that of the right lobe ("LL derived").
• Characteristic pattern Within a given genus the bursal pattern usually varies among the species. Moreover, as seen immediately above, most species have a different pattern in each lobe. This means that in some genera we can find several different patterns. However it seems possible to choose one or two characteristic patterns for each Review Parasite, 2012, 19, 3-18 genus. The characteristic pattern is determined by the type most frequently found, which is here interpreted as the most frequent basic type plus the contiguous intermediary types. For example, for the genus Sciurodendrium Durette-Desset, 1971 (Pudicinae, seven species) we propose that the characteristic pattern is of type 2-2-1 because amongst the 11 treatable lobes, four are of type 2-2-1, three of type 2-3 t 2-2-1, and two of type 2-2-1 t 1-3-1. Some genera may have two characteristic patterns. For example in Heligmonina (Nippostrongylinae, 27 species) two characteristic patterns are proposed: 1-3-1 and 1-4; type 1-3-1 being the most frequent in the right lobe and type 1-4 in the left lobe (21 and 19 lobes respectively). . Sciuricola Durette-Desset, 1983 (2/2) CB SS. CB with different patterns in both lobes (1 sp.). Patterns observed: 2-3 t 2-2-1, atypical 1-2-1-1. Characteristic pattern: the data are insufficient to choose a characteristic pattern but two characters of the CB shared by both species are rays 4 and 5 separated from base and dorsal lobe distinct.
On the other hand, its synlophe is also very different from that of the remaining species in the genus. It is likely that this species belongs to a different genus and it is not treated herein.
.  (Hasegawa, Miyata & Syafruddin, 1999), O. similis Smales, 2009 andO. uromyos (Mawson, 1961    Based on the elements considered above, the four subfamilies may be synthetically characterized as follows: the Heligmonellinae by a subsymmetrical caudal bursa, with the same pattern in both lobes, and a characteristic pattern of type 2-2-1 (Table I); the Brevistriatinae by a predominantly subsymmetrical caudal bursa, a right/left ratio which is variable but with predominantly the same pattern in both lobes, and several types of pattern with a predominance of the characteristic type 2-2-1 (Table II); the Pudicinae by a subsymmetrical caudal bursa, a right/left ratio which is variable but with predominantly the same pattern in both lobes, and several types of patterns with a predominance of characteristic types 2-2-1 and 1-4 (Table III) is also variable and several types of pattern with a predominance of characteristic types 2-2-1 and 1-4 (Table IV).

DISCUSSION
O f the five main patterns recognized among the Trichostrongylina treated by Durette-Desset (1985), only three were observed in the Heligmonellidae: 2-3, 2-2-1 and 1-3-1. In this article, the main feature considered was the grouping of the rays and, in the interpretation of its evolution, only two main tendencies were considered: the shortening of the dorsal ray and the lengthening of rays 4. 1-3-1 2-2-1 1-4, 2-2-1, 1-3-1 1-3-1 RL, 1-4 LL 2-2-1 1-3-1 2-2-1 1-4 2-2-1 2-3 2-2-1 2-3 2-2-1 2-3 t 2-2-1 1-3-1, 4-1 RL 4-1, 3-1-1 LL 2-2-1, 1-4 2-2-1 2-2-1, 1-4 2-2-1 2-2-1 2-2-1 1-4 2-2-1,  In the present article, we provide an additional feature at the descriptive level, which is the sequence of the origin of the rays from the common trunk. Consequently, the presence of a new basic pattern (type 1-4) is highlighted, plus the presence of intermediary types: type 2-3 tending to 2-2-1, type 2-2-1 tending to 1-3-1, type 1-3-1 tending to 1-4 and type 2-2-1 tending to 1-4, which have enabled us to attempt an evolutionary interpretation of the patterns. Type 2-3, the basal type, is somewhat infrequent, but not the following intermediary type, 2-3 t 2-2-1, which is common and present in all four subfamilies. The basic type, 2-2-1, seems to be the most consistent pattern in the family: it is the most frequent characteristic pattern, is present in all four subfamilies, and there are relatively few intermediary types from 2-2-1 to 1-3-1, to 1-4 or to atypical patterns. Types 1-3-1 and 1-4 are less frequent than type 2-2-1 but are characteristic of several genera; type 1-3-1 is observed in all four subfamilies, and is the origin of several atypical types (4-1, 3-1-1, 1-2-2 and 1-2-1-1); type 1-4, characteristic of laterally elongated lobes, is absent from the Heligmonellinae. Finally, the family Heligmonellidae is characterized by the fact that, regardless of the pattern, with very few exceptions, rays 4 and 5 are always the last to diverge from the common trunk of rays 2 to 6. It is clear that a dissymmetrical or asymmetrical caudal bursa should be regarded as derived with respect to a subsymmetrical one. However, the type of symmetry has been actually considered a character of little value above the species level, since the asymmetrical bursae and mostly the dissymmetrical bursae have arisen several times during the course of evolution. The dissymmetry usually involves the transverse (lateral) lengthening of one of the lobes. This dissymmetry probably plays a role in holding the female during copulation (Durette-Desset, 1985). The most conspicuous asymmetries and dissymmetries are found among the Nippostrongylinae. In species with a slight dissymmetry the lengthening may or may not modify the bursal pattern, which usually remains the same in both lobes. In species with strong dissymmetry, species, which are usually tightly coiled spirally, the pattern is usually different for each lobe. Independent of the type of symmetry, both lobes of the caudal bursa may have the same or different patterns. In the latter case the most frequent situation from an evolutionary point of view is one lobe having one pattern and the other lobe showing the "next" intermediary or basic type (e.g. Neoheligmonella 2-3 t 2-2-1 and 2-2-1; Heligmonina 1-3-1 and 1-4); there are very few cases in which both lobes have a totally different pattern (e.g. Heligmonella asymmetrica, some species of Stilestrongylus). Review Parasite, 2012, 19, 3-18 In some genera the same "right/left ratio" is observed in all or most species in the genus: either both lobes have the same pattern (Heligmostrongylus, Pudica), or it is always the same lobe, which is derived with respect to the other (Heligmonina). Other genera are less homogeneous and the right/left ratio varies among the species of the genus (Neoheligmonella, Paraheligmonina).

Genus
The combination of the right/left ratio and type of symmetry gives disparate results: in genera with marked dissymmetry or asymmetry, the hypertrophied lobe is usually the same but it may show either the derived pattern (Heligmonina, LL) or the basal pattern (Nippostrongylus, RL). In genera with subsymmetrical or slightly dissymmetrical caudal bursae, not only may the right/left ratio vary but also the type of symmetry within each genus (Odilia, Paraheligmonina).
It is interesting to note that the Heligmonellinae, the Brevistriatinae and the Pudicinae, in which most of the caudal bursae are subsymmetrical with the same pattern in both lobes, are parasitic in hosts, which are relatively ancient (mainly sciuromorph and caviomorph rodents, a few in insectivores and lagomorphs). The Nippostrongylinae, in which the symmetry and the pattern in both lobes are more variable, are parasitic in a group, which appeared more recently, the muroid rodents (mainly cricetids and murids).