Sexual conflict and sympatric speciation in the Pacific

A project undertaken at the School of Biological, Earth and Environmental Sciences, University of New South Wales, and supervised by Dr Nikolai Tatarnic

INTRODUCTION

Conflict between males and females over mating is thought to fuel intense evolutionary arms races between the sexes, through a process known as sexually antagonistic coevolution (SAC) (1). SAC is thought to drive rapid evolutionary change in morphology and behaviour (2), and has even been invoked as a vehicle for speciation (3, 4).


In the plant bug genus Coridromius, mating takes place by traumatic insemination (TI): males bypass the female genital tract, instead stabbing their partners with hypodermic genitalia and ejaculating into their blood (5). In response, females of many TI species have evolved elaborate paragenitalia at the site of copulation to reduce the costs of mating. TI was first discovered in bedbugs (6) and is thought to have arisen either as a means for males to circumvent female mating resistance or as a product of male-male competition (4, 7). TI is an incontrovertible example of a conflict trait, as males obligatorily damage females to promote their own reproductive success, and females coevolve paragenitalia to reduce these costs.


In our recent revision of Coridromius (8) we identified several unique and elaborate paragenital forms and increased the number of described species from 11 to 33, with many of these found throughout the South Pacific. In particular, New Guinea has been identified as an area of endemism for the genus, with eight described species thus far, all collected in the same region. For this project we will travel to the Kamiali Research Station in Papua New Guinea to study various aspects of sexual conflict and speciation in Coridromius. This field station is the ideal site for this research, as the region is known to harbour high diversity of Euphorbiaceae, the prime host plants for the genus.


RESEARCH AIMS

The goals of this project are as follows:
  1. Collect fresh material of new and already described species from PNG. These will provide valuable DNA material necessary for phylogenetic reconstruction and to estimate relative times of divergence (i.e. speciation). In PNG we find many related species living in sympatry, yet indications from other species surprisingly suggest little ecological divergence across the genus.
  2. Examination of the functional morphology of female paragenitalia. Fresh specimens will allow us to identify internal organs involved in TI, and compare these to what is known in bedbugs.
  3. Through digital video recordings we will document for the first time the biology and mating behaviour of these species. No species of Coridromius with elaborate paragenitalia has been observed mating and in some cases the paragenitalia are so bizarre we cannot comprehend their function without direct observation.
  4. To compare the mating behaviour of species with complex and simple paragenitalia. We predict that in simple species females will struggle vigorously, while in complex species there will be little or no struggling, as mating costs are negated by the paragenitalia.
  5. To measure costs of TI, we will compare the longevity of singly vs. multiply mated females of different species. We predict that simple species will suffer greater reduction in longevity than complex females.
  6. Using a phylogeny, we will trace the evolution of paragenitalia, behaviour and costs across the genus. As well, we will explore the possibility of sympatric speciation among PNG species.
OUTCOMES

Through this project we anticipate the following outcomes:

  1. Establish the evolutionary relationships of Coridromius species from PNG.
  2. Describe for the first time the life history and mating behaviour of these bizarre insects.
  3. Determine the functional significance of paragenital structures in Coridromius, and relate these to what is known in other TI systems.
  4. Through optimization of measures of cost and behaviour across the phylogeny, evaluate the evolution of paragenital elaboration in Coridromius under the predictions of sexually antagonistic coevolution.
  5. Using all our results, assess the possibility that sexual conflict has lead to rapid reproductive isolation and speciation in Coridromius species of PNG.
RECENT PROGRESS

Antagonistic coevolution:
We have recently reconstructed a phylogeny of all known Coridromius species, based on 67 morphological characters.  Using this phylogeny and phylogenetically independent contrasts, we have shown that male genitalia and female paragenitalia are coevolving: in those species where the male intromittent organ differs from a simple scythe shape (e.g. is twisted, thickened, laterally compressed, etc), this is matched by paragenital modifications in the female (Tatarnic & Cassis 2010). We speculate that the males’ modifications might reflect increased puncturing strength of the intromittent organ, possibly in response to increased cuticular thickness at the site of intromission in females. This is currently being explored.


Sympatric speciation:
We are currently amassing fresh specimens in order to develop a total evidence phylogeny based on both morphological and molecular data. Molecular information will provide crucial branch length estimates which are needed in assessing the influence of sexually antagonistic coevolution on speciation. We have successfully obtained molecular sequence data from 10 species of Coridormius thus far, and hope to extend this data set with further sampling in the coming year.
Mating behaviour:
Mating behaviour has been observed in 4 species of Coridromius to date. All of these species are “simple”, i.e. lacking elaborate female paragenitalia. In these species females struggle vigorously in an attempt to dislodge their would-be suitors. In the coming year we will document whether or not those species with elaborate paragenitalia struggle less, indicating that the costs of traumatic insemination have been mitigated by their biology rather than through behavioural response.

REFERENCES   
  1. Parker, G.A. 1979. Sexual selection and sexual conflict. In Sexual selection and Reproductive Competition in Insects (eds. M. S. Blum, N. A. Blum), pp. 123-166. London: Academic Press.
  2. Chapman, T., Arnqvist, G., Bangham, J. and Rowe, L. 2003. Sexual Conflict. Trends in Ecology and Evolution 18: 41-47.
  3. Gavriletts, S. 2000. Rapid evolution of reproductive barriers driven by sexual conflict. Nature 403: 886-889.
  4. Arnqvist, G. & Rowe, L. 2005. Sexual conflict. In Monographs in Behavior and Ecology (ed. J. R. Krebs & T. H. Clutton-Brock). Princeton, NJ: Princeton University Press.
  5. Tatarnic, N.J., Cassis, G. and Hochuli, D.F. 2006. Traumatic insemination in the plant bug genus Coridromius Signoret (Heteroptera: Miridae). Biology Letters 2(1): 58-61.
  6. Carayon, J. 1966. Traumatic insemination and paragenital system. In R. L. Usinger (ed). Monograph of Cimicidae (Hemiptera, Heteroptera). Entomological Society of America, College Park, MD: pp. 81-166.
  7. Reinhardt, K., and Siva-Jothy, M.T. 2007. Biology of the bedbugs (Cimicidae). Annual Review of Entomology 52: 351-374.
  8. Tatarnic, N.J. and Cassis, G. 2008. Revision of the plant bug genus Coridromius Signoret (Insecta: Heteroptera: Miridae). Bulletin of the American Museum of Natural History 315: 1-95.
  9. Tatarnic, N.J. and Cassis G. 2010. Sexual coevolution in the traumatically inseminating plant bug genus Coridromius. Journal of Evolutionary Biology 23: 1321-1326.
Figure 1. Correlated male (left) and female (right) reproductive morphology of Coridromius nakatanii (above) and C. sommelieri (below). In both of these species, the male intromittent organ is complemented by a sclerotized copulatory tube in the female.

Figure 2. Phylogeny of Coridromius, showing distinct Eastern (red) and Western (yellow) clades. Numbers above branches indicate bootstrap and jackknife support values, numbers below are Bremer indices.

Figure 3. Coridromius hermosus from Papua New Guinea.