This new observation of phoretic copulation in S. pensylvanica is recognized as an opportunity to critically review the published information regarding mating strategies in Mutillidae and to develop new terminology that accurately describes them. Data on the mating strategies for 62 mutillid species are comprehensively reviewed in Table 1. References that merely note a pair being collected in copula, or copulating in captivity, were excluded. These observations are numerous in the literature and usually provide no additional information other than the sex association itself. In compiling these data, it became apparent how little is known overall on the mating behavior of the family, especially behavior documented in natural settings. Observations of mating events in captivity have been deemed problematic, as males will attempt to mate with non-conspecific and even non-congeneric females (Ferguson 1962; Manley 1977; Manley and Pitts 2007). Copulation behavior and mating time observed in the laboratory may not be congruent with behavior that would normally occur in the field. The observations cited in Table 1 as being conducted in captivity should be kept with this in mind. The higher classification of Mutillidae in this contribution follows Brothers and Lelej (2017), except Dolichomutilla Ashmead, 1899 is considered a member of Mutillini rather than Trogaspidiini, and the two apparent genus-groups that comprise the Mutillini subtribe Ephutina (the Ephuta genus-group and the Odontomutilla genus-group) are considered full tribes within Mutillinae (Ephutini and Odontomutillini, respectively). These partial modifications in classification are used here in anticipation of a molecular phylogeny of Mutillidae using Ultra-Conserved Elements (Waldren et al. in prep.).

As mentioned previously, there have been two types of mating strategies recognized in mutillids: phoretic copulation and in situ copulation. Two subtypes of phoretic copulation were recognized by Brothers (1989). One was termed “true phoretic copulation” wherein the male initially uses his legs to pick up a female and once terminalic union occurs, phoresy is strictly effected by the genitalia and surrounding metasomal structures; mating occurs during flight or while nectaring. Within Mutillidae, this first subtype is known to occur in the myrmosine tribe Myrmosini and the subfamily Rhopalomutillinae (Table 1). “True phoretic copulation” also occurs in some subfamilies of Bethylidae and Thynnidae (Evans 1969; Osten 1999; Azevedo et al. 2016). The other subtype is known to commonly occur in the subfamily Mutillinae (excluding Mutillini and Odontomutillini) and now in Sphaeropthalminae (S. pensylvanica) (Table 1), wherein the female is primarily supported by the male’s mandibular clasp around her pronotal neck, and secondarily by his legs and terminalic union. The pair travels from the initial site of contact by male flight and/or foot and eventually settle on a substrate to finish mating (Nonveiller 1980; Brothers 1989; Brothers and Finnamore 1993). However, this second subtype is technically also “true phoretic copulation,” as the female is carried by the male with his mandibles throughout the mating event, even while the pair are resting on a substrate in copula (Nonveiller 1980; Cambra and Quintero 1993; Bartholomay et al. 2017; Cambra et al. 2018; current study). Active transport by flight while in copula is not required for the mating event to be considered “true phoretic copulation.”

In order to accurately characterize these patterns of behavior, new terminology is proposed with respect to Mutillidae to broadly define the two types of mating strategies currently known to occur in the family. 1) Phoretic Copulation (PC) is a form of phoresy in which a male intentionally carries a female phoront for the majority of their mating event. There are two subtypes of phoretic copulation: 1a) Terminalic Phoretic Copulation (TPC) is phoresy primarily effected by terminalic union (i.e. the genitalia and surrounding structures) between a male and a female phoront for the majority of their mating event (secondarily with his legs) (Fig. 6). 1b) Mandibular Phoretic Copulation (MPC) is phoresy primarily effected by a male’s mandibular clasp around a female phoront’s pronotal neck for the majority of their mating event (secondarily with his legs and terminalic union) (Figs 2–4, 7). 2) In Situ Copulation (ISC) is a non-phoretic mating event that occurs at or near the site of initial contact between a male and a female (Fig. 5).

In ISC, there are some observations of males clinging to the dorsum of females during part of the mating event and even clasping their mandibles around the female’s pronotal neck (Cottrell 1936; Ferguson 1962; Bayliss and Brothers 1996, 2001); these events are not considered phoretic copulation as intentional carriage by the male does not occur. This behavior in the context of ISC may play a role in courtship, recognition of conspecificity between the sexes, and/or the biomechanics of mating. Subtypes of ISC may potentially be defined at a later date once more data are available. Mating duration for species that practice PC is often considerably longer than species that practice ISC (Table 1); consequently, mating pairs are collected more often in PC-practicing taxa (Mickel 1937; Nonveiller 1980). The observation described herein for S. pensylvanica is considered MPC.

A potential third subtype of phoretic copulation was described by O’Toole (1975) for the trogaspidiine species Wallacidia oculata (Fabricius, 1804) and congeners. As was described: “The posture of copulation in [W.] oculata is venter to venter, with the male uppermost. The female clings to the sides of the male mesosoma, with the tarsal claws gaining purchase on the coarse sculpture of the male.” This mating position is unusual, as most known mating observations in Mutillidae occur with the male venter to female dorsum (although sometimes with wide separation between the male and female’s bodies except for the terminalia). In contrast to this mating posture description, O’Toole (1975) also provided evidence that MPC occurs in W. oculata and the now full species Wallacidia melmora (Cameron, 1905): “I have seen several pairs of [W.] o. melmora in museum collections in which the females are in the mandibular clasp of the males. J. Cardew (personal communication) found a male of [W.] o. oculata with a female in its mandibles, at Chang Mai, Thailand.” There are two additional published records that describe a venter to venter mating position in the TPC-practicing Myrmosini species Myrmosa atra Panzer, 1801 and M. unicolor Say, 1824. As detailed in Krombein (1956), both K. V. Krombein and H. K. Townes had independently observed mating pairs of M. unicolor in the field that were oriented venter to venter. Additionally, Saxton (2010) observed a mating pair of M. atra oriented venter to venter. Prior to the pair’s separation, the couple assumed an end to end mating position and Saxton (2010) determined that the male’s genitalia must have rotated 180° to a facultative strophandrous position (sensu Schulmeister 2001). Male genitalic rotation is also known to occur in the TPC-practicing Thynnidae that engage in male to female feeding (Evans 1969; Vivallo 2020). In contrast to these records, Cambra et al. (2018) included a photograph of a pair of M. unicolor that remained in copula after being collected in a Malaise trap which are in a male venter to female dorsum position. An online search for photographs of mating pairs of Myrmosini revealed that females’ bodies are rotated to various degrees with respect to the male. One of these photographs of a mating pair of M. unicolor is included here (Fig. 6) and shows a roughly 90° rotation of the female’s body.

For Myrmosini, variable female mating position and likely male genitalic rotation are supported by observations in the field by multiple researchers. For Trogaspidiini, information on venter to venter mating is limited to O’Toole (1975). It is unknown whether this mating posture was observed with live specimens or if it was inferred from museum specimens. If the description in O’Toole (1975) was based on preserved material, the venter to venter posture of the mating pair might be an artifact of how the collector mounted the specimens (and might be how the collector envisaged the posture of the mating pair during the act if they happened to terminate copulation and separate upon being captured). Further, a photograph of a mating pair of W. oculata is included in this study (Fig. 7) and they are practicing MPC. We ultimately regard the venter to venter mating position described in O’Toole (1975) as erroneous. All known mating descriptions suggest trogaspidiines practice MPC (Table 1) and the available evidence supports that Wallacidia species are no different.

Figures 5–7. 

Examples of each type of mating strategy in Mutillidae 5 ISC, Dasymutilla foxi (Cockerell, 1894) in Arizona, USA; photograph by Mark H. Brown 6 TPC, Myrmosa unicolor Say, 1824 in New York, USA; photograph by A. D. Levine 7 MPC, Wallacidia oculata (Fabricius, 1804) in Southern District, Hong Kong; photograph by ‘aabbabc.’

Sexual dimorphism in size, with the male being larger than the female, is an important criterion for phoretic copulation to effectively occur (Nonveiller 1963; Deyrup and Manley 1986; Brothers 1989; Tormos et al. 2010; Matteini Palmerini 2013). This size dimorphism is in contrast with other parasitoid Hymenoptera wherein females are commonly larger than males (Charnov et al. 1981; O’Neill 1985; Hurlbutt 1987; van den Assem et al. 1989). In some taxa that are known to normally practice MPC, some male individuals are similar or smaller in body size to the female they are mating with and are physically unable to transport her by flight or even by foot; facultative ISC consequently occurs (Nonveiller 1963; Alicata et al. 1975; Deyrup and Manley 1986; Tormos et al. 2010; Matteini Palmerini 2013; Polidori et al. 2013). It is unknown if the reverse situation also occurs wherein a species that normally practices ISC due to similarity in male and female size might practice facultative MPC with unusually large males. In evidence against the latter situation, Cottrell (1936) observed that for Dasymutilla bioculata (Cresson, 1865), a sphaeropthalmine species that practices ISC, larger males were mechanically unable to copulate with smaller females. Females are often larger than males in this species, and mating was successful when smaller males mated with larger females. Additionally, male aptery and brachyptery, which are uncommon in Mutillidae (Cambra and Quintero 2007, 2017), would limit phoretic copulation by flight but not by foot; mating behavior for species with flightless males has yet to be observed, though. The cause of adult intra- and intersexual size differences within a mutillid species is primarily predicated upon host choice.

Mutillids are generally solitary ectoparasitoids that may parasitize more than one host species. It has long been known that the size of the host determines the size of the adult mutillid, which explains the common occurrence of adult size variation (Mickel 1924; Deyrup and Manley 1986; Brothers 1989; Hennessey 2002). If a female mutillid parasitizes more than one host species that vary in size in relation to one another, her offspring will consequently vary in size. In some mutillid taxa, one sex is on average larger than the other, and the underlying mechanics for sex allocation in mutillids remained unknown until relatively recently. Of critical relevance to the new discovery of phoretic copulation in S. pensylvanica is an investigation into sex allocation in this species by Pitts et al. (2010a). Their results supported facultative size-dependent sex allocation in which males typically develop from larger hosts and females develop from smaller hosts. Due to the sex-determination system of haplodiploidy in Hymenoptera, female S. pensylvanica are able to choose whether to oviposit a fertilized or unfertilized egg onto a specific host. Unfertilized eggs, which develop into males, are more often deposited on larger hosts, such as the organ pipe mud dauber Trypoxylon politum (Drury, 1773) (Hymenoptera: Crabronidae); female eggs are usually deposited on smaller Trypoxylon species and other taxa (Matthews 1997; Pitts et al. 2010a). Pitts et al. (2010a) concluded that female S. pensylvanica likely use host body length and/or nest diameter as criteria for which sex of egg—male or female—to oviposit on a host rather than the criterion of host mass. The difference in size between the male and female mating pair of S. pensylvanica documented herein is substantial (Figs 2–4), and the size dimorphism prerequisite for phoretic copulation is clearly met. Although a rare occurrence, female S. pensylvanica have been reared from T. politum and males reared from smaller Trypoxylon species (Pitts et al. 2010a). More mating observations are necessary for S. pensylvanica to see how mating is carried out, if at all, between these smaller males and larger females. Facultative size-dependent sex allocation is likely widespread among PC-practicing mutillids due to the importance of intersexual size dimorphism.

The genus Sphaeropthalma Blake, 1871 is a paraphyletic assemblage of 81 described species classified into 17 species-groups (Pitts et al. 2010b; Pitts and Sadler 2015). Sphaeropthalma pensylvanica (Lepeletier, 1845) is currently placed in the S. pensylvanica species-group along with S. auripilis (Blake, 1871), S. boweri Schuster, 1944, and S. nocticaro Pitts, 2005 (Pitts and Sadler 2015). Given that these other members of the species-group also show the same differences in body size between the sexes, it is likely that they practice MPC as well. Unfortunately, the females of most of the remaining Sphaeropthalma species, as well as the related large genera Photomorphus Viereck, 1903 and Odontophotopsis Viereck, 1903, are unknown. The known females are closer in size to the males and there seem to be no other likely candidates for MPC in Sphaeropthalma outside of the S. pensylvanica species-group or the related genera Photomorphus and Odontophotopsis.

There are a few unusual distributions in Sphaeropthalminae that might be due to dispersal via PC. Sphaeropthalmines primarily occur in the Nearctic, Neotropical, and Australasian regions, with two small genera occurring in the Palaearctic (Europe, China, Japan, Republic of Korea) and Oriental (China, Taiwan) regions. These latter two genera, Cystomutilla André, 1896 and Hemutilla Lelej, Tu, & Chen, 2014 were recently reviewed by Tu et al. (2014). Molecular data has revealed that Cystomutilla is closely related to the nocturnal Nearctic Sphaeropthalminae (Waldren et al. in prep.). The practice of phoretic copulation, which has, in part, been hypothesized to aid the apterous females in traversing physical barriers such as water (Evans 1969), is not out of the realm of possibility in Cystomutilla and Hemutilla in light of the behavior being discovered in S. pensylvanica. Another genus in which PC may have played a role in dispersal is the primarily Australian genus Ancistrotilla Brothers, 2012. Several species are known to occur in New Caledonia and one in Vanuatu, an archipelago of volcanic origin (Brothers 2012; Lo Cascio 2015). The only species known so far from both sexes, Ancistrotilla azurea Brothers, 2012, which occurs in Vanuatu, meets the size prerequisite for phoretic copulation with males being larger than females. Additionally, the single known female was apparently collected in the same Malaise trap as fifteen males and could potentially have been carried into the trap by a male.