Overcoming an evolutionary conflict: Removal of a reproductive organ greatly increases locomotor performance

Abstract

One potential consequence of sexual size dimorphism is conflict among characters. For example, a structure evolved for reproduction can impair performance during other activities (e.g., locomotion). Here we provide quantitative evidence for an animal overcoming an evolutionary conflict generated by differential scaling and sexual size dimorphism by obligatorily removing an undamaged reproductive organ, and thus dramatically enhancing its locomotor performance. The spider genus Tidarren (Araneae, Theridiidae) is interesting because, within several species presenting extreme sexual size dimorphism (males representing Ϸ1% of the total mass of the female), males voluntarily remove one of their two disproportionately large pedipalps (modified copulatory organs; a single one represents Ϸ10% of the body mass in an adult) before achieving sexual maturity. Whether the left or right pedipalp is removed appears to be random. Previous researchers have hypothesized that pedipalp removal might enhance locomotor performance, a prediction that has remained untested. We found that, for male Tidarren sisyphoides, maximum speed increased (44%) significantly and endurance increased (63%) significantly after pedipalp removal. Furthermore, spiders with one pedipalp moved Ϸ300% greater distances before exhaustion and had a higher survival after exertion than those with two pedipalps. Removal of the pedipalp may have evolved in male Tidarren because of enhanced abilities to search for females (higher endurance and survival after exertion) and to out-compete rival males on the female's web (higher maximum speed). Our data also highlight how the evolution of conflicts can result in the evolution of a novel behavior.A central tenet of optimality theory is that natural selection will optimize structure and performance resulting in an overall highly fit organism (1, 2). Many studies, however, have shown that the evolution of high performance in one task can lead to decreased performance during another task (e.g., refs. 3-5). In extreme cases of such apparent conflicts, a structure evolved for one activity can substantially impair performance during another activity. For example, Darwin (6) described how sexual selection for sex differences might lead to such functional conflicts, particularly in males. He depicted how the relatively elaborate feathers in some male birds result in enhanced reproductive success via female mate choice, yet also reduces or constrains flight capacities, thus potentially making the animal more susceptible to predators (7). A relatively unexplored area is how organisms cope with these constraints imposed by factors such as sexual selection, natural selection, or allometry. One view of constraints is that they limit or hinder morphological or behavioral change, but another possibility is that constraints can result in a novel phenotype or behavior (8, 9). For example, as plethodontid salamanders undergo evolutionary miniaturization (become smaller), they shift from a terrestrial to an arboreal lifestyle (10). This ...

Females prefer to associate with males with longer intromittent organs in mosquitofish

“…Basolo & Alcaraz 2003) and genitalia (House & Simmons 2003). Locomotor costs of nonretractable genitalia occur in G. affinis (Langerhans et al 2005) and spiders (Ramos et al 2004).…”

Have Male and Female Genitalia Coevolved? A Phylogenetic Analysis of Genitalic Morphology and Sexual Size Dimorphism in Web-Building Spiders (Araneae: Araneoidea)

“…Such large pedipalps may be maintained because they ensure a fit to the much larger female copulatory apparatus (Vollrath 1998). If so, these spiders appear to have resolved the conflict by self-amputating one of their two overly large pedipalps, and thus considerably enhancing both maximum speed and endurance (Ramos et al 2004). In sum, different and even opposing scaling trends in sexual genitalic and size dimorphism could have profound consequences for reproduction and life history of spiders, and perhaps other taxa as well.…”

“…The spider Tidarren sisyphoides is highly size dimorphic (the male is 1% of the total female body weight) and male palps are large enough (about 10% of their total body weight) that they substantially hinder locomotion (Ramos et al 2004). Such large pedipalps may be maintained because they ensure a fit to the much larger female copulatory apparatus (Vollrath 1998).…”

Emasculation: gloves-off strategy enhances eunuch spider endurance

“…Tidarren sisyphoides males emasculate one palp before mating, whereas N. malabarensis males break off their palps during mating. It is unclear whether N. malabarensis eunuchs' superior fighting abilities [14] are also directly related to increased endurance capacity after the removal of their disproportionately large palps [16], i.e. the 'gloves-off ' hypothesis [12].…”

“…However, proximate mechanisms behind better fighting abilities in eunuchs remain unknown. A previous study on Tidarren sisyphoides found that males were more agile and mobile showing higher endurance (time until exhaustion) after palp removal, because the palp represents a disproportionally high body weight share [16]. Tidarren sisyphoides males emasculate one palp before mating, whereas N. malabarensis males break off their palps during mating.…”