The evolution of mating systems in bark and ambrosia beetles (Coleoptera: Scolytidae and Platypodidae)

Abstract

The extraordinary array of mating systems in the Scolytidae and Platypodidae has been largely overlooked by researchers interested in the evolution of sexual behaviour. This paper provides the first overview of reproductive behaviour in this important and widespread group, known to most biologists only by the reputations of tree-killing taxa. Referred to generally as ‘bark beetles’, these insects chew egg tunnels inside a variety of (usually dead) plant tissues, though most species are either phloeophagous (breeding in the inner bark of woody plants) or xylomycetophagous (all stages feeding on mutualistic fungi growing on sapwood or heartwood). In most species, permanent records of many aspects of reproductive behaviour are etched in the host; in many, engravings reveal female fecundity, eggs sired per male, hatching success, and offspring survivorship. Each gallery arm represents a good portion of a given female's lifetime reproduction, but in many species females commonly re-emerge to reproduce in one or two additional sites. In most species of bark beetles, each female initiates her own gallery, to be joined later by a male. These monogynous gallery systems are associated with mating systems defined by how long males stay with females: in a few species, males seldom if ever join females under the bark; in the vast majority of species, males stay for part or all of the oviposition period then leave to seek other mates; and a few groups exhibit permanent monogamy, in that both sexes die in their only gallery system. While these patterns emerge from an overview of the world scolytid fauna, the length of male residency has seldom been quantified, and the costs and benefits associated with male mating strategies have not been measured for any bark beetle. Male-initiated monogyny is uncommon in Scolytidae, though the rule in Platypodidae; all instances of which I am aware are summarized from a phylogenetic perspective. Inbreeding polygyny with highly biased sex ratios has arisen at least seven times in Scolytidae. These taxa are usually characterized by males being dwarfed, flightless, and uncommon. Sex determination is known for only a few examples, but both haplodiploidy and diplodiploidy have been reported. Multiple origins of harem polygyny (otherwise rare in invertebrates) add an exciting dimension to the comparative and experimental study of scolytid mating systems. In harem polygynous taxa, males initiate gallery construction. I summarize what little can be learned from the literature about the fine structure of harem polygynous mating systems in bark beetles, and the problem of measuring reproductive success. Data on the nature of harem polygyny in Pityophthorus lautus are presented, illustrating (a) the fluidity of harems; (b) that average eggs laid per gallery arm is relatively unaffected by harem size, but strongly influenced by resource quality; (c) that male egg-gain is strongly correlated with territory quality (a consequence of (b) above); and (d) the temporal patterning of immigration and emigration and its effects on gallery system sex ratios. The second half of this paper is a discussion of the evolution of bark and ambrosia beetle mating Mating systems, emphasizing sexual selection and the role of resources. Male, residence is interpreted as postcopulalory guarding-preventing sexual liaisons with wandering males. Operational sex ratio, encounter rate, synchrony of breeding, ejaculate competition, and spatiotemporal distribution of resources are discussed as evolutionary forces moulding scolytid and platypodid male postmating behaviour. The nature of male male competition is reviewed. The paucity of information on male behaviour in gallery systems is mentioned; whether or not males significantly aid females is not known. Three hypotheses are presented for why females re-emerge, a feature which strongly affects operational sex ratios. Finally, I summarize features of bark beetle existence predisposing them to the evolution of post-inseminative guarding. Male-initiated monogyny presents a puzzle. I propose that most uncontested examples can be explained by monogyny re-evolving from (male-initiated) harem polygyny, and I present an argument for the evolution of harem polygyny leading to the development of male gallery initiation. The evolution of harem polygyny in birds and mammals has attracted considerable attention. The Verner Willson Orians polygyny threshold model is discussed with respect to bark beetles in general and P. lautus in particular. Resource quality is a major factor in P. lautus harem dynamics: the cost to females of joining harems is apparently slight compared to benefits accrued from moving into sites with higher quality inner bark. Female-biased adult sex ratios have been suggested to lead to harem polygyny, and literature and original data pertinent to this hypothesis are examined. The geometric constraints model, based on the polygyny threshold concept but tailored to bark