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The evolution of antennal courtship in diplazontine parasitoid wasps (Hymenoptera, Ichneumonidae, Diplazontinae).

Klopfstein S, Quicke DL, Kropf C - BMC Evol. Biol. (2010)

Bottom Line: As predicted by theory, traits associated with reproduction often evolve at a comparatively high speed.On the basis of a well-resolved phylogeny, we reconstruct the evolutionary history of antennal coiling and associated morphological modifications to study the mode of evolution of this complex character system.Further studies are needed to ascertain whether the loss of antennal coiling is irreversible on larger timescales, and whether evolutionary constraints have influenced courtship behavioural traits in a similar way in other groups.

View Article: PubMed Central - HTML - PubMed

Affiliation: Natural History Museum (Invertebrates), Bernastrasse 15, CH-3005 Bern, Switzerland. klopfstein@nmbe.ch

ABSTRACT

Background: As predicted by theory, traits associated with reproduction often evolve at a comparatively high speed. This is especially the case for courtship behaviour which plays a central role in reproductive isolation. On the other hand, courtship behavioural traits often involve morphological and behavioural adaptations in both sexes; this suggests that their evolution might be under severe constraints, for instance irreversibility of character loss. Here, we use a recently proposed method to retrieve data on a peculiar courtship behavioural trait, i.e. antennal coiling, for 56 species of diplazontine parasitoid wasps. On the basis of a well-resolved phylogeny, we reconstruct the evolutionary history of antennal coiling and associated morphological modifications to study the mode of evolution of this complex character system.

Results: Our study reveals a large variation in shape, location and ultra-structure of male-specific modifications on the antennae. As for antennal coiling, we find either single-coiling, double-coiling or the absence of coiling; each state is present in multiple genera. Using a model comparison approach, we show that the possession of antennal modifications is highly correlated with antennal coiling behaviour. Ancestral state reconstruction shows that both antennal modifications and antennal coiling are highly congruent with the molecular phylogeny, implying low levels of homoplasy and a comparatively low speed of evolution. Antennal coiling is lost on two independent occasions, and never reacquired. A zero rate of regaining antennal coiling is supported by maximum parsimony, maximum likelihood and Bayesian approaches.

Conclusions: Our study provides the first comparative evidence for a tight correlation between male-specific antennal modifications and the use of the antennae during courtship. Antennal coiling in Diplazontinae evolved at a comparatively low rate, and was never reacquired in any of the studied taxa. This suggests that the loss of antennal coiling is irreversible on the timescale examined here, and therefore that evolutionary constraints have greatly influenced the evolution of antennal courtship in this group of parasitoid wasps. Further studies are needed to ascertain whether the loss of antennal coiling is irreversible on larger timescales, and whether evolutionary constraints have influenced courtship behavioural traits in a similar way in other groups.

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Estimated transition rates between coiling states. (A) Transition rates between the three states of coiling behaviour as estimated by maximum likelihood. (B) Posterior distribution of rates obtained from Bayesian analysis. States are: 0 = no coiling, 1 = single coiling, 2 = double coiling.
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Figure 4: Estimated transition rates between coiling states. (A) Transition rates between the three states of coiling behaviour as estimated by maximum likelihood. (B) Posterior distribution of rates obtained from Bayesian analysis. States are: 0 = no coiling, 1 = single coiling, 2 = double coiling.

Mentions: Overall, the rate of evolution of both morphological and behavioural characters was rather low, as indicated in Figure 3 for antennal coiling. The consistency (CI) and retention index (RI) of presence and absence of both tyloids and coiling behaviour indicated low levels of homoplasy (CI = 0.333 and RI = 0.931 for tyloids and CI = 0.500 and RI = 0.960 for coiling behaviour). To further study the mode of evolution of antennal coiling in Diplazontinae, we examined more closely the estimated transition rates between the two states, especially, whether the rate of change from the state 'absent' to 'present' (rate0- > 1) was equal to zero. To this end, we restricted the transition rates to being either all equal or one of them being zero, and compared the outcomes to the unrestricted case with two different transition rates. Under the unrestricted model, the rate0- > 1 was estimated to be zero, and this model had the highest likelihood. However, when compared to the equal rates model, this increase in likelihood was not significant with the likelihood ratio test (LRH = 1.61, df = 1, p = 0.20). The posterior probability of rate0- > 1 being zero was estimated as 72% by the MCMC approach, which integrates over phylogenetic uncertainty. When taking the mode of antennal coiling into account, ML estimations confirm a zero rate for the transitions 0- > 1 and 0- > 2, as shown in Figure 4A. The corresponding posterior probability distributions obtained from the Bayesian analysis are shown in Figure 4B.


The evolution of antennal courtship in diplazontine parasitoid wasps (Hymenoptera, Ichneumonidae, Diplazontinae).

Klopfstein S, Quicke DL, Kropf C - BMC Evol. Biol. (2010)

Estimated transition rates between coiling states. (A) Transition rates between the three states of coiling behaviour as estimated by maximum likelihood. (B) Posterior distribution of rates obtained from Bayesian analysis. States are: 0 = no coiling, 1 = single coiling, 2 = double coiling.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2927921&req=5

Figure 4: Estimated transition rates between coiling states. (A) Transition rates between the three states of coiling behaviour as estimated by maximum likelihood. (B) Posterior distribution of rates obtained from Bayesian analysis. States are: 0 = no coiling, 1 = single coiling, 2 = double coiling.
Mentions: Overall, the rate of evolution of both morphological and behavioural characters was rather low, as indicated in Figure 3 for antennal coiling. The consistency (CI) and retention index (RI) of presence and absence of both tyloids and coiling behaviour indicated low levels of homoplasy (CI = 0.333 and RI = 0.931 for tyloids and CI = 0.500 and RI = 0.960 for coiling behaviour). To further study the mode of evolution of antennal coiling in Diplazontinae, we examined more closely the estimated transition rates between the two states, especially, whether the rate of change from the state 'absent' to 'present' (rate0- > 1) was equal to zero. To this end, we restricted the transition rates to being either all equal or one of them being zero, and compared the outcomes to the unrestricted case with two different transition rates. Under the unrestricted model, the rate0- > 1 was estimated to be zero, and this model had the highest likelihood. However, when compared to the equal rates model, this increase in likelihood was not significant with the likelihood ratio test (LRH = 1.61, df = 1, p = 0.20). The posterior probability of rate0- > 1 being zero was estimated as 72% by the MCMC approach, which integrates over phylogenetic uncertainty. When taking the mode of antennal coiling into account, ML estimations confirm a zero rate for the transitions 0- > 1 and 0- > 2, as shown in Figure 4A. The corresponding posterior probability distributions obtained from the Bayesian analysis are shown in Figure 4B.

Bottom Line: As predicted by theory, traits associated with reproduction often evolve at a comparatively high speed.On the basis of a well-resolved phylogeny, we reconstruct the evolutionary history of antennal coiling and associated morphological modifications to study the mode of evolution of this complex character system.Further studies are needed to ascertain whether the loss of antennal coiling is irreversible on larger timescales, and whether evolutionary constraints have influenced courtship behavioural traits in a similar way in other groups.

View Article: PubMed Central - HTML - PubMed

Affiliation: Natural History Museum (Invertebrates), Bernastrasse 15, CH-3005 Bern, Switzerland. klopfstein@nmbe.ch

ABSTRACT

Background: As predicted by theory, traits associated with reproduction often evolve at a comparatively high speed. This is especially the case for courtship behaviour which plays a central role in reproductive isolation. On the other hand, courtship behavioural traits often involve morphological and behavioural adaptations in both sexes; this suggests that their evolution might be under severe constraints, for instance irreversibility of character loss. Here, we use a recently proposed method to retrieve data on a peculiar courtship behavioural trait, i.e. antennal coiling, for 56 species of diplazontine parasitoid wasps. On the basis of a well-resolved phylogeny, we reconstruct the evolutionary history of antennal coiling and associated morphological modifications to study the mode of evolution of this complex character system.

Results: Our study reveals a large variation in shape, location and ultra-structure of male-specific modifications on the antennae. As for antennal coiling, we find either single-coiling, double-coiling or the absence of coiling; each state is present in multiple genera. Using a model comparison approach, we show that the possession of antennal modifications is highly correlated with antennal coiling behaviour. Ancestral state reconstruction shows that both antennal modifications and antennal coiling are highly congruent with the molecular phylogeny, implying low levels of homoplasy and a comparatively low speed of evolution. Antennal coiling is lost on two independent occasions, and never reacquired. A zero rate of regaining antennal coiling is supported by maximum parsimony, maximum likelihood and Bayesian approaches.

Conclusions: Our study provides the first comparative evidence for a tight correlation between male-specific antennal modifications and the use of the antennae during courtship. Antennal coiling in Diplazontinae evolved at a comparatively low rate, and was never reacquired in any of the studied taxa. This suggests that the loss of antennal coiling is irreversible on the timescale examined here, and therefore that evolutionary constraints have greatly influenced the evolution of antennal courtship in this group of parasitoid wasps. Further studies are needed to ascertain whether the loss of antennal coiling is irreversible on larger timescales, and whether evolutionary constraints have influenced courtship behavioural traits in a similar way in other groups.

Show MeSH
Related in: MedlinePlus