Female mate preferences can evolve for exaggerated male traits that are indicators of male quality [1
]. In resource-free mating systems in which males only provide females with ejaculates, it is often assumed that choosy females benefit through indirect genetic benefits to their offspring [2
]. However, ejaculates vary in the amount of accessory substances as well as the number and quality of sperm transferred, and these constituents are important determinants of female fertility, fecundity and longevity [3
]. Consequently, if male ornamentation also signals ejaculate quality, this is likely to be an additional force favouring the evolution of female mate preferences.
In this paper, we investigate whether male ornamentation signals reproductive quality in the stalk-eyed fly Teleopsis dalmanni
(synonym Cyrtodiopsis dalmanni
]), in particular, the ability of males to confer fertility. There is evidence that variation in fertility is an important component of female fitness in T. dalmanni
. Multiple copulations are required by females to achieve and maintain high fertility [5
]. This is probably because of the small size of the male spermatophore [6
] and the small number of sperm stored following a single copulation (approximately 65 [8
]). This effect is compounded by X-linked meiotic drive, which is found in 13–17% of field collected males [9
]. Meiotic drive impairs the development of Y-bearing sperm, causing lowered fertility in females mated to drive males [10
]. Consistent with these findings, less than 40% of eggs laid by field-caught females failed to hatch, though the exact cause of this has yet to be established [12
Male reproductive quality is associated with the size of the accessory glands and testes. These internal reproductive organs are very small at eclosion, and then dramatically increase in size, allowing males to attain sexual maturity three to four weeks later [13
]. Accessory gland growth rate is positively correlated with the time required to reach sexual maturity [13
] while the size of the mature accessory glands is both phenotypically [13
] and genetically [15
] correlated with male mating frequency. The ability of a male to mate multiply is likely to be an important contributor to female fertility, as matings are concentrated in the periods shortly before dusk and after dawn when single males mate with several females [16
]. Testis size is positively correlated with the number of sperm stored in a female's spermathecae following copulation [17
] and thus is also likely to affect female fertility.
A number of experiments have established that females prefer to roost and copulate with males with larger eyespan [18
]. Hence it is possible that male eyespan acts as a signal of male reproductive quality and so leads to elevated fertility in choosy females. Note however that while eyespan is a highly condition-dependent trait which is sensitive to environmental stress during larval development [21
], external morphology is fixed at eclosion [24
]. This seems likely to limit the effectiveness of eyespan as a signal of accessory gland and testis size as these traits are strongly influenced by environmental stress during their maturation in adult flies [13
]. Consequently there is a compelling need to explicitly investigate whether male eyespan predicts the growth and size at maturity of the internal reproductive organs, and whether it influences female fertility.
The possibility that fertility assurance is a major selective force in the evolution of female mate preferences for exaggerated male sexual ornaments has been discussed most extensively under the heading of the "phenotype-linked fertility hypothesis". This hypothesis originally linked fertility assurance to extra-pair matings in socially monogamous birds [25
] but has since been generalized to all cases where sexual ornaments covary with male fertility traits [27
]. More recently, the idea has been framed within the handicap principle, with the implication that the covariance between male ornaments and fertilizing efficiency arises because both are condition-dependent traits [29
]. So males in good condition not only develop more attractive ornaments but also make greater investment in male fertility traits.
Empirical evidence for the hypothesis is ambiguous [27
]. For example, studies using commercial strains or commercial/wild hybrids of domestic fowl have largely supported the hypothesis [29
], whereas no relationship between male comb size and testis size was found in a captive population of Red Jungle fowl, the conspecific ancestor of domestic fowl [32
]. The strongest support for the phenotype-linked fertility hypothesis comes from Wagner & Harper's [33
] study of field crickets. Male chirp rate is positively correlated with the number of sperm transferred and females mated to males with higher chirp rates exhibited higher lifetime fertility. However, Wagner & Harper [33
] may have exaggerated the importance of this finding as females were restricted to a single mating; given the opportunity, female field crickets normally remate at high frequency [34
]. Furthermore, positive results were only observed in females fed a restricted diet; females fed a standard diet received no fertility benefits from males with high chirp rates.
In this paper we consider three fundamental requirements for the phenotype-linked fertility hypothesis to be supported. First, the male ornament or display must be subject to female mate preference. Second, attractiveness of the male ornament or display must be positively correlated with appropriate measures of male reproductive quality. This relationship needs to be made across the range of environments encountered in natural populations, as associations between fitness components can disappear or reverse direction in different environments [35
], so single environment measures could be misleading. Third, females that mate with males possessing exaggerated ornaments or displays must exhibit higher fertility than females that mate with males with lower trait values. Otherwise positive correlations between ornament expression and male reproductive traits are not likely to be relevant to the issue of adaptive female preference [37
In T. dalmanni
, directional female preference for large eyespan males has already been documented [17
], so we did not investigate it further here. We examined whether male eyespan was positively correlated with the growth of the accessory glands and testes as a way of gauging variation in male reproductive quality. These relationships were measured under a range of nutritional regimes, which cause environmental stress during adult development. We then tested whether females mated to large eyespan males exhibited higher fertility than females mated to small eyespan males.