Research Focus:
Sexual Selection, Speciation & Drosophila Genitalia

Why genitalia?

Rapid evolutionary divergence of male genital morphology represents one of the most striking trends across animal taxa with internal fertilization. In many cases, genitalia provide taxonomically useful characters for distinguishing between organisms at the species level, often where no other morphological trait will suffice (Eberhard 1985). This pattern appears to be extraordinarily general, although it has been suggested that biases in taxonomic methods may have influenced the extent to which this is considered to be a general phenomenon, and exceptions have been documented (Huber 2003, Bond et al 2003). Genital evolution has fascinated biologists for over 150 years (Dufour 1844), yet detailed intraspecific studies of genitalia remain scarce and many pertinent issues remain unresolved
(Arnqvist 1997, Hosken & Stockley 2004).

What are genitalia?

The choice of criteria with which to define male genitalia is troublesome (Darwin 1871). For convenience, the term is applied to mating structures contacting the female on or near her gonopore. This definition incorporates secondary intromittent devices such as the pedipalps of some invertebrates, spermatophores that males of some groups deposit outside of their bodies and then use
instead of or in addition to the intromittent organ and also additional copulatory structures such as claspers. Such structures display the pattern of rapid and divergent
evolution (Eberhard 1985).

What are the causes of genital evolution?

Three main hypotheses have been proposed to explain the morphological diversification of animal genitalia.

Reproductive Isolation: Genital divergence is under selection for mechanical species isolation, preventing maladaptive hybridization, via ‘lock-and-key’ or ‘genitalic recognition’ (Dufour 1844, Shapiro & Porter 1989, Eberhard 1985).

Pleiotropy: Genitalia are selectively neutral and evolve via pleiotropic effects of selection on other traits (Mayr 1963). Alternatively, pleiotropy initiates divergence in one sex, which leads to intersexual coevolution of genital structures between the sexes, under natural selection for morphological correspondence (Arnold 1973).

Sexual Selection: Optimal genital structures confer a reproductive advantage on individuals bearing them (Short 1979, Eberhard 1985). This hypothesis has been subdivided into four distinct mechanisms (Hosken & Stockley 2004); sexual conflict (Trivers 1972, Parker 1979, Lloyd 1979, Alexander et al 1997), ‘runaway’ (Fisher 1915), ‘good genes’ (Zahavi 1975) and sperm competition (Parker 1970).

Are genitalia important traits in sexual selection?

Understanding the evolution of mating biases is a longstanding goal in ecology and evolution (Kokko et al 2003). The widespread nature of rapid and divergent genital evolution suggests that an understanding of its significance might yield especially valuable insight into the relative merits of alternative theoretical models of sexual selection (Eberhard 1993). Evidence from studies of macroevolutionary pattern and microevolutionary process provides support for the hypothesis that postcopulatory sexual selection is important in driving genital diversification (Short 1979, Waage 1979, Eberhard 1985, Arnqvist 1998, Hosken & Stockley 2004). Interesting research has also highlighted the potential importance of natural selection and precopulatory sexual selection in genital evolution (Ramos et al 2004, Langerhans et al 2005).

Traditional models of mating biases are based upon mutualistic interactions between the sexes (Fisher 1915, Zahavi 1975). Interest has recently focused upon the possibility that sexual conflict (Trivers 1972, Parker 1979, Chapman et al 2003) can drive sexual selection through an evolutionary arms race referred to as sexually antagonistic coevolution (Holland & Rice 1998). This conceptual shift has been stimulated to a large extent by the identification of harmful male reproductive traits, including genital morphology that damages the female reproductive tract during copulation (Crudgington & Siva-Jothy 2000). The unambiguous distinction between mutualistic and antagonistic interactions in sexual selection has thus far proved rather elusive and a lively debate is currently concerned with determining the relative importance of each using theoretical and empirical approaches (Chapman et al 2003, Hosken & Snook 2005 and references therein).

Theory predicts that sexual ornaments and weapons can evolve isometry, positive and negative allometry, as is consistent with the observed diversity of static allometric patterns in nature (Bonduriansky & Day 2003). Genitalia sometimes display negative static allometry and low phenotypic variation, particularly in invertebrates, and this has lead to the proposal of the ‘one size fits all’ hypothesis whereby male genitalia are under stabilizing selection to fit the average female (Eberhard et al 1998). Positive genital allometry and high phenotypic variation has been observed in other taxa, often vertebrates (Lupold et al 2004). Such patterns offer insight into trait evolution and have been interpreted as evidence in support of particular modes of sexual selection (Bonduriansky & Day 2003, Eberhard et al 1998, Hosken & Stockley 2004).

What are the consequences of genital evolution?

Interest has grown in the potential for the evolution of reproductive traits to generate reproductive isolation and speciation (Panhuis et al). This includes traits evolving under postcopulatory sexual selection at the cellular and molecular levels, such as gamete morphology and reproductive proteins, which consistently display more rapid diversification than non-reproductive equivalents (Birkhead & Pizzari 2002). Traditionally favoured hypotheses, proposing that genital divergence is under selection as a mechanism of hybridization avoidance,
have obtained little support (Shapiro & Porter 1989). Reproductive isolation and speciation might, however, occur as a consequence of genital evolution (Sota & Kubota 1998, Cordero Rivera et al 2004).

Shown in left lateral view are the aedeagus, aedeagal apodeme and paraphysis of D. guacamaya (a), D. papei (b), D. periquito (c), D. ranchograndensis (d), D. tschirnhausi (e), D. merzi (f), D. pittieri (no aedeagus shown) (g) and D. luisserrai (h). Scale bars 100mm. (From Hosken & Stockley 2004, originally published by Bächli& Vilela 2002, Vilela & Bächli 2002).

How can this problem be approached?

I aim to test hypotheses for the causes and consequences of genital evolution by employing a multidisciplinary approach focusing on flies of the genus Drosophila as a model lineage. Fruit flies are exciting because their reproductive physiology, mating behaviour, systematics and genetics have been well studied.  This enables a combination of phylogeny-based comparative methods and experimentation, including experimental evolution in the laboratory. Sophisticated methodologies are also available for the characterization of Drosophila genital apparatus. The potential for future research into the genetic basis of genital evolution is another tantalizing prospect.

Diagrammatic sketches of Drosophila genitalia (From Vilela 1983) (a) Male genitalia, lateroblique aspect:
A microtrichia; B cercus; C epandrium; D surstylus;
E prensisetae; F inner setae; G outer setae;
H gonopod; I hypandrium; J aedeagus; K suture; L aedeagal apodeme.
(b) Aedeagus, aedeagal apodeme and outer paraphyses lateroblique aspect: M tip; N dorsal cleft; O dorsal margin; P ventral rod; Q outer paraphysis; R ventral margin. prospect

 

 

Drosophila starmeri: a  (strain W-12) male genitalia, lateroblique aspect; b-d(strain W-17), aedeagus, aedeagal apodeme and outer paraphyses, several aspects.
(From Vilela 1983).

 

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