Chapter 5. Reproductive skew in Parischnogasteralternata
(Vehrencamp, 1983; Reeve a/., 1993, Kokko et a l, 1999; Ragsdale, 1999) and tug-of- war (Reeve etal., 1998a) models to explaining skew in primitively eusocial wasps is also discussed. This discussion is mainly confined to primitively eusocial wasps for several reasons. Principal among these is that the concession and tug-of-war models were primarily developed with primitively eusocial wasp societies in mind (Reeve & Ratnieks, 1993; Reeve et al., 1998a). Furthermore, to date skew has not been directly quantified for many species (Heinze, 1995; Bemasconi, 1997; Bourke et al., 1997; Field et al., 1998a; Lundy et al., 1998; Reeve é ta l, 2000; Cooney & Bennett, 2000; Eggert & Muller, 2000; Heinsohn e ta l, 2000; Fournier & Keller, 2001; Heinze et a l, 2001; Haydock & Koenig, 2002; Seppa et a l, 2002; Sumner e ta l, 2002), and direct attempts to test the skew models have mainly been confined to primitively eusocial wasps (Field et a l, 1998a; Reeve et al,
2000; Seppa et al., 2002; Sumner et al, 2002). Social structures also differ markedly among the social insects, ranging from primitively eusocial species in which a single female founds a nest and then proceeds to progressively feed her brood, to large colonies of ants, bees, and wasps which may have one to several queens and hundreds (in some species millions) of workers (Wilson, 1971). In large social insect colonies workers may play a key role in determining the number of queens and their relative contributions to colony reproduction (Keller & Vargo, 1993). This means that the factors affecting skew ariiong queens in large social insect colonies may not necessarily be analogous to the factors effecting skew among members of a primitively eusocial colony (Reeve & Keller, 2001). In a recent review. Reeve and Keller (2001) concluded that concession models generally explain observed patterns of reproduction in small-colony social insects better than any other existing model. Most of the evidence was indirect, as only two studies that have attempted to directly test the predictions of the skew models (both on paper wasps) had been published at the time (Field et a l, 1998a; Reeve et al., 2000). Since the publication of this review two more studies have been published (Seppa et al., 2002; Sumner et a l, 2002). Therefore, along with the analysis presented in this thesis, skew has now been studied in five species of primitively eusocial wasp (Field et a l, 1998a; Reeve et
Chapter 5. Reproductive skew in Parischnogasteralternata a l, 2000; Seppa et at., 2002; Sumner et a l, 2002). In the following text these studies are compared and discussed with regard to the concession and tug-of-war models.
P. altematacompared with L. flavolineata
Sumner et al. ’s (2002) study on L. flavolineata can be directly compared with the analysis presented in this thesis on P. altematahQcmse. both studies utilized similar procedures and used the corrected 5’ index to calculate skew (Keller & Krieger, 1996). The average skew
in P. altemata (0.92 ± 0.051, 9 nests) is similar to that cdculated for L. flavolineata (S =
0.95 ± 0.033, 13 nests). Furthermore, in L. flavolineata, skew among female eggs was found to be 1.0 in 11 out of 13 nests (84.62%), while in P. altematais was 1.0 in seven out of nine nests (77.78%). Therefore, in both species, the production of female brood is nearly always monopolized by a single female. In general, the genetic structure of L.
flavolineata colonies is similar to that presented in this thesis for P. altemata (Section
3.4.4). In both species, nest-mates tend to be close relatives, although on average they are not sisters, colonies may contain several non-overlapping sibgroups, and reproduction is nearly always monopolized by a single female at any one time. It is known for L.
flavolineata that subordinates queue for the position of reproductive dominance and that
nest inheritance is common(Shreeves & Field, 2002). The evidence collected in this study suggests that P. altemata subordinates may also be positioned in an age-based queue for inheritance of the nest. However, in L. flavolineata the likelihood of the dominant being the mother of all male eggs was zero (10% of the male eggs were not laid by the dominant) (Sumner, 1999; Sumner et al., 2002). Sumner et al. (2002) suggested that in L.
flavolineata subordinates may sometimes be daughters of the dominant and would
therefore on average be more closely related to the dominant’s female offspring than to her male progeny. They suggested that this may explain why subordinate females tend to produce sons rather than daughters. A maximum likelihood analysis performed in this study suggested that P. altemata dominants were likely to be the mother of all the young male progeny. However, the power of this analysis was low as it was performed on only seven nests that contained a total of 12 brood. In regard to the skew models, Sumner et al.
Chapter 5. Reproductive skew in Parischnogasteralternata
(2002) came to similar conclusions for L. flavolineata as were made here for P, altemata
(Section 5.4.2). They concluded that skew in L. flavolineata cannot be explained by any compromise models, but may be explained by concession models that consider the benefits of future breeding (Kokko & Johnstone, 1999; Ragsdale, 1999; Sumner et a l, 2002).
Tropical hover wasps compared to temperate paper wasps
Paper wasps unlike stenogastrines have annual colony cycles. The typical paper wasp life cycle is as follows. In spring, overwintered inseminated females begin colonies, either alone or in groups. In multiple foundress associations, a single female is usually behaviourally dominant, producing most of the eggs and rarely leaving the nest. The other females forage for food to provision the first cohort of brood which usually become workers, although an individual from a worker cohort may become the replacement queen. Later in the season the following year’s reproductives are produced. These mate, and mated females hibernate over the winter period ready for the following season (Reeve,
1991; Nonacs & Reeve, 1995).
In all three species of paper wasp for which reproductive partitioning has been studied to date (P. bellicosus (Field et a i, 1998a); P. fuscatus (Reeve et al., 2000); P. Carolina
(Seppa et a l, 2002)), average skews in reproductive brood are high, although they tend to be lower and more variable between nests, compared to the uniformly high skews that have been observed in the stenogastrines P. altemataand L. flavolineata (Sumner, 1999; Sumner a/., 2002). Furthermore, in all three paper wasp species average skew in early brood was lower than skew in brood produced later in the nesting season (Table 5.7). Collectively, these results suggest that a positive association between increasing skew and colony age may be typical of temperate paper wasp species.
Chapter 5. Reproductive skew in Parischnogasteralternata
Table 5.7. Comparison of average skews between early and late brood cohorts in three paper wasp species.
Species Early brood Late brood Dataset Reference
P. bellicosus 0.49 ± 0.07 0.68 ± 0.07 Reproducing females only Field 1998a
P. fuscatus 0.70 ± 0.05 0.93 ± 0.08 Full-sister foundress associations
Reeve era/., 2000
P. Carolina 0.54 ± 0.06 0.65 ± 0.04 All foundresses Seppaera/., 2002
Reeve et al. (2000) explained the positive correlation of skew with colony age they observed in P. fuscatus within a concession based framework. They suggested that skew increases with time because subordinates require smaller staying incentives, since the probability of a subordinate nesting independently and producing any reproductives before the season ends decreases as the colony cycle progresses. However, Seppa et al. (2002) have suggested for P. Carolina that the parentage of early brood may not be critical, as these zu^e destined to become workers that will not obtain any direct reproduction. Instead of reproducing directly, these workers will help provision the late progeny that become the following year’s reproductives. Therefore, to the dominant, the maternity of the workers may not be important, providing they help raise her brood of reproductives. These two contrasting perspectives on temporally increasing skew highlight a problem with investigating reproductive partitioning in temperate species. The line separating reproductive from non-reprodutive skew may be blurred (Reeve & Ratnieks, 1993). Although, in temperate paper wasp species, all adult females may be physiologically capable of reproduction, the time of their emergence may determine whether or not they are destined to become, and remain, as helpers. For P. fuscatus. Reeve et al. (1998b) have provided evidence that some of the early brood cohort reproduce as replacement queens and that many become foundresses the following year. However, late brood may still have more reproductive value to foundresses than early brood (Reeve & Keller, 2001).
Chapter 5. Reproductive skew in Parischnogasteralternata
Nevertheless, regardless of this contentious issue of whether or not early brood in paper wasps should be considered as reproductive or non-reproductive brood, a temporal pattern in reproduction among paper wasp foundresses appears to exist, suggesting that reproduction is increasingly monopolized by the dominant females as the colony cycle progresses.
In the stenogastrines P. altemata (this study) and L. flavolineata (Sumner, 1999; Sumner et al., 2002), reproduction was monopolized by a single female in nearly all colonies examined. In these species, in contrast to the temperate paper wasps, reproduction may always be monopolized by a single female irrespective of colony age. This may be because hover wasps inhabit a relatively aseasonal environment where nest initiation occurs throughout the year and colonies may survive indefinitely (Samuel, 1987).
In P. altemataskew was 1.0 in seven of nine nests. Although, it was not possible to age
these colonies, it seems unlikely that they were all initiated at the same time of year. Furthermore, if skew changed during the year, but happened to be high when the nests were collected, lower skew among the older brood cohorts should have been found. However, this was not the case. In 12 of 15 colonies, reproduction was found to have been monopolized by a single female irrespective of brood age (Section 5.3.1). For this reason, in P. altemata as in L. flavolineata, reproduction is probably performed exclusively by a single female, regardless of colony age or time of year. Therefore, there appear to be clear differences in patterns of reproduction between the tropical stenogastrines and the temperate paper wasps. Firstly, skew in the three paper wasp species tends to be lower and more variable between nests compared to the uniformly high skew of P. altemata and
L. flavolineata. Secondly, reproduction within nests of the three paper wasp species is
increasingly monopolized by a single female as the colony cycle progresses, while in P,
altemataa.nd L. flavolineata colonies, skew is nearly always 1.0 irrespective of colony age
or time of year.
Sumner et al. (2002) have suggested that differences in breeding regimes may explain the lower more variable skew found in the temperate paper wasps compared to the high invariable skew they observed in L. flavolineata. Stenogastrines inhabit tropical regions
Chapter 5. Reproductive skew in Parischnogasteralternata
and may therefore be relatively unrestricted by seasonal changes. In a relatively aseasonal tropical environment the chance of a female inheriting the position of dominance is probably little affected by the time of year that she emerges. However, for temperate wasps such as some Polistes species, the chance of a female inheriting (the position of dominance) and successfully breeding will decrease as the breeding season progresses. This is because as the breeding season progresses, the amount of time available for breeding decreases (Reeve, 1991). Furthermore, if dominance is determined by a conventional cue such as age, the later in the colony cycle a female emerges, the further down the queue for inheritance she will be. Sumner et al. (2002) have suggested that the small group sizes, extended colony cycles and absence of seasonal constraints on breeding in the tropical hover wasps, may be reflected in a female’s choice of reproductive strategy. Therefore the high invariable skew observed in the tropical hover wasps compared to the lower more variable skew of the paper wasps may be explained by female hover wasps choosing to wait to inherit dominance, as they can afford to wait longer than the seasonally restricted temperate wasps. However, this suggestion of Sumner et a l/s (2002) does not give any theoretical explanations for why skew should differ. For example, in the stenogastrines skew is high, supposedly because females have a chance of inheriting the nest. In the paper wasps, amongst late brood skew is also high (although less so that in the hover wasps), although females late in the season have little chance of inheriting reproduction, unless some are the following year’s reproductives (Reeve et a i, 1998b). A speculative concession based explanation for these patterns of skew is as follows. In the stenogastrines, skew may be invariably high because subordinates can afford to wait to inherit reproduction. Therefore, subordinates are not given a staying incentive in the form of direct reproduction as they have a good chance of inheriting the nest along with its work force. Therefore, in a sense, their staying incentive comes in the form of future reproduction (as in Kokko and Johnstone’s (1999) and Ragsdale’s (1999) models). In the temperate paper wasps, skew increases as the colony cycle progresses because the probability of successful independent nesting by subordinates decreases. As the colony cycle progresses, the size of the staying incentives given to paper wasp subordinates by
Chapter 5. Reproductive skew in Parischnogasteralternata
dominants will decrease (Reeve et at., 2000). Subordinates may continue to help raise the young of their relatives because the indirect fitness gained by helping is greater than the direct fitness to be obtained by nesting independently. Furthermore, later in the colony cycle subordinates may have little choice but to remain as helpers, unless they become reproductives the following year (Reeve et al, 1998b).
Skew models
Three studies on paper wasps have tested predictions of skew models (Field et al., 1998a; Reeve e/a/., 2(X)0; Seppa etal., 2002). Of these analyses, only Reeve et aV s (2(X)0) has provided any support for the predictions of the concession models (Reeve & Ratnieks, 1993). In their study. Reeve et al. (2000) found skew to be positively correlated with relatedness, colony productivity and aggression as predicted by Reeve and Ratnieks (1993) concession model (Section 4.2.1). However in contrast to Reeve et al. ’s (2(X)0) results, in their study on P. bellicosus. Field et al. (1998a) found that relatedness either did not predict skew or was negatively correlated with it, a result that matches the prediction of Reeve et al.’s (1998a) restricted access tug-of-war model, and not Reeve and Ratnieks’ (1993) concession model. Field et al. (1998a) also found that in contrast to Reeve and Ratnieks’ (1993) concession model, high skew was associated with decreased aggression. However, this result is in agreement with Cant and Johnstone’s (2000) extended analysis of fighting ability and skew which predicts that higher relatedness usually leads to lower levels of aggression (Section 4.2.1). In Field et al.'s (1998a) study, within-nests cofoundresses were related on average by 0.67 ± 0.035 which is just below full-sister relatedness of 0.75. Field et al. (1998a) did not investigate the potential effect of group productivity on skew. In P. Carolina, Seppa et al. (2002) found that skew was not correlated with relatedness, colony productivity or aggression. Therefore, support for the concession model in paper wasps is sparse. In the stenogastrines, P. altemata and L.
flavolineata (Sumner et al., 2002) skew was uniformly high, nearly always being 1.0
while the putative explanatory variables (relatedness, group size, and per capita productivity) were found to be significantly more variable than skew. This suggests that
Chapter 5. Reproductive skew in Parischnogasteralternata
skew is nearly always 1.0 irrespective of these parameters. Although these results do not appear to support the concession model they can be explained within a concession based framework, provided constraints on independent nesting were strong and subordinates gain some indirect fitness benefits from helping (Vehrencamp, 1983; Reeve & Ratnieks, 1993; Kokko & Johnstone, 1999; Ragsdale, 1999; Sumner et a l.y 2002; Section 5.4.2).
However, the results of the stenogstrine studies do not provide any positive evidence in support of the concession models. With regard to the tug-of-war models (Reeve et al. , 1998a), these analyses are not applicable to the stenogastrines because strictly speaking, under the assumptions of these analyses, skew can never be 1.0, because dominants do not have complete control of group reproduction (Section 5.4.2). Furthermore, tug-of-war analyses assume that dominants are better fighters than subordinates. This assumption may not be met in P. altemata or L. flavolineata ( Sumner et a l, 2002), as dominance in these species appears to be determined by age. Of the paper wasp studies, only Field et
a l/s (1998a) provides any support for the tug-of-war models, that being the finding
mentioned above that relatedness either was not affected by, or decreased with skew. Dominance in some paper wasp species appears to be generally settled by conventional cues (Queller et al., 1997; Seppa et a i, 2002). Therefore, the assumption of the tug-of- war models that dominants are better fighters than subordinates may not be met by the paper wasps either. Therefore, tug-of-war models are unlikely to be suitable for explaining patterns of reproduction in the paper wasps.
From this brief survey of the direct studies that have been performed on primitively eusocial wasps, it would appear that Reeve and Keller’s (2001) conclusion that concession models generally explain observed patterns of reproduction in small-colony social insects may be premature. Of the five skew studies that have been performed to date on primitively eusocial wasps, only one provides compelling evidence in support of the concession model, that being Reeve et a i ’s (2000) study on P. fuscatus.
Certain aspects of the skew models may not be relevant to primitively eusocial wasps. This might explain why the skew studies have yielded only sparse support for the concession models. For example, if a relationship between relatedness and skew is to be
Chapter 5. Reproductive skew in Parischnogasteralternata
observed within a single population or even species, individuals must have the ability to recognise levels of kinship (Hogendoom & Velthuis, 1999). Although, it is generally acccepted that colony-members can discriminate between nest-mates and non-nest-mates, it is not known whether social insects are able to assess degrees of relatedness (Queller e/ at.,
1990; Keller, 1997; Quellere/a/., 2000). If social insects are unable to measure levels of relatedness, theoreticians will need to develop new models built on different assumptions. If this is done, the predictions of the models may then change. It has also been suggested by Hogendoom and Velthuis (1999), and Sumner et al. (2002) that the relatedness aspect of the concession model may be more relevant at the species or population level than at the colony level. If individuals are not able to assess degrees of relatedness, then the average population relatedness may be important in shaping skew, but a relationship between relatedness and skew will not be found within a population. If this is the case then the effect of relatedness on skew can only be examined by comparing populations or species.
In this study it has been suggested that the uniformly high skew in P. altematamay be explained by concession models that consider future breeding benefits (as resource inheritance may be important in this tropical species ) (Kokko & Johnstone, 1999; Ragsdale, 1999). In fact, prospects of future breeding are likely to be important in explaining skew in most species. For example, in P. fuscatus skew has been found to vary with the stage of the breeding season (Reeve et al., 2000). Efforts at explaining skew using models which do not consider future breeding prospects may be extremely limited.