A new study using artificial selection reveals that the size of the sex comb on the legs of male flies is genetically correlated with their fertility success under conditions of sperm competition

Pomiankowski, A

Wedell, N

English

UCL Discovery

 1 DISPATCH, Current Biology 2021, volume 31, R478-481 Sexual selection: Large sex combs signal male triumph in sperm competition  Andrew Pomiankowski 1,2* and Nina Wedell3  1 Department of Genetics, Evolution and Environment, University College London, Gower Street, London, WC1E 6BT, UK 2 CoMPLEX, University College London, Gower Street, London, WC1E 6BT, UK 3 Biosciences, University of Exeter, Penryn Campus, Penryn TR10 9FE, UK * E-mail: ucbhpom@ucl.ac.uk   A new study using artificial selection reveals that the size of the sex comb on the legs of male flies is genetically correlated with his fertility success under conditions of sperm competition.    As spring hits the animal world, out come gaudy lures, whirling dances, potent smells, shrieks and yelps as males — and sometimes females — attempt to attract liaisons, brief or prolonged, with the opposite sex. Males are happy to trade investment in sexual displays for gains in reproduction. Females compare and assess displays to gain benefits for themselves and their offspring. Where direct gains (food, nests, territory) are absent, genetic endowment is usually invoked as the profit of the female gaze, even though it has proven hard to establish beyond reasonable doubt. A plausible alternative is that ornaments directly indicate male fertility, his ability to sire a large brood, triumph in competition against other males’ ejaculates and pass on potent sperm production to sons in the next generation. Unfortunately, this idea, branded the "phenotype-linked fertility hypothesis"1, remains contentious for a simple reason: the more  2 desirable a male, the more he mates and the less he has to invest per mating2. Fertility benefits aren't fixed, they inevitably are diluted, especially among more attractive, multiply mating males3-5. A recent study in Current Biology, by Michal Polak and colleagues6 challenges this pessimistic view by new experimental evidence on the sex combs of the fly Drosophila bipectinata (Figure 1).   Males use sex combs, teeth-like bristles on their front legs, to gently grasp and caress their partners’ abdomens in pre-copulatory foreplay. Females respond favourably and proceed to copulation when stimulated by well-endowed males sporting larger combs. To uncover what advantages females gain from their mate choice, artificial selection was applied to comb size on D. bipectinata flies collected from the field. Comb size showed high heritability, with average tooth number going from a baseline of 13 to 16 in the high and 10 in the low selected lines (anaesthetize 100 males, and repeatedly pick the 30% highest or lowest). After 11 generations of selection, males from the lines were tested in a classic ‘P2’ sperm competition experiment. Standard females were mated first to an irradiated stock male and then to the focal test male. Irradiation was set to a sub-lethal dose which leaves sperm able to fertilise, but embryos die due to lethal mutations. The proportion of eggs producing offspring after the second mating (P2) reflects the competitive fertilizing success of the second test male. In males from the lines selected for high comb number, P2 was strongly elevated.   ` Artificial selection thus beautifully uncovered an underlying genetic correlation between comb size and male fertilizing success. The obvious mechanistic reason for this association is that larger combs cause greater female arousal and preferential sperm use, so called cryptic female choice. However, this explanation was cleverly dismissed by Polak and colleagues6. They used a fine scale laser to ablate individual teeth from the sex combs of high-line males,  3 bringing the number down to low-line levels. To their surprise, this phenotypic manipulation had no impact on competitive fertilization success. Ablated high-line males achieved elevated P2, no different from their non-ablated relatives. What can be baldly stated is that the experimentally induced difference in sex comb size simply does not explain preferential fertilization success.  A number of other candidate traits that might explain the greater fertilization success of high-line males were ruled out by Polak and colleagues6. Body size is often correlated with fertility, as it was also here. But as the artificial selection regime controlled for size, there was no difference between lines. Increased male mating rate, testis size and accessory gland size all seem good candidates for the higher fertilization success, but none of these were greater in high-line males. More promising, a comparison of mRNA transcripts identified three ejaculate proteins transferred from the male accessory glands to the female at mating that were upregulated in high-lines. Fortunately, these proteins have been previously studied in Drosophila melanogaster. One of these proteins is the well-known sex peptide, which has a range of effects on female sexual behaviour including suppressing their propensity to remate and enhancing male siring success in sperm competition7,8. The other two are serine proteases that enhance male fertility9. Exactly how these ejaculate components work in D. pectinata is not known. They appear to increase high-line sperm viability when extracted from the female's ventral receptacle, a cassette-like structure where sperm are individually stored before release into the oviduct. To survive in this location, male ejaculates contain a diversity of proteins that confer resistance to female spermicidal secretions10. This might explain why upregulation of these proteins is associated with increased high-line sperm competitiveness.  A key question posed by the results is the reason for the unravelled genetic association between a sexual ornament and fertilizing capacity. Polak and colleagues6 suggest that  4 attractive males more often encounter intensive sperm competition. This should lead to selection shaping their ejaculates to cope with competitive environments, much more so than the ejaculates of undesirable males. Sperm competition theory certainly supports the idea that competition favours larger or more potent ejaculates with greater ‘fertilizing power’ when competition increases11. But this prediction is based on population-level comparisons, where there are particular male types, for example territory-holders and satellites, which differ radically in their opportunities to mate12. This selective logic might apply in D. pectinata if males adorned with large combs excite previously mated females to re-mate earlier in their sexual cycle, well before the female has exhausted sperm stored from previous males. Then, ejaculates of large-comb males will typically encounter greater numbers of rival sperm and will profit from greater investment in costly seminal proteins to overcome them. However, it remains to be shown whether females are indeed more willing to remate when encountering highly ornamented males as suggested. This explanation predicts that the greater ‘offensive’ capabilities (second male success) of attractive males does not carry over to ‘defence’ against rival sperm (ability to withstand competition from subsequent ejaculates) as the ‘strength’ of subsequent male ejaculates is not predictably linked to the current male's attractiveness. This prediction is yet to be examined.   There are more generic concerns about the notion that male sexual ornaments are associated with greater fertility13. Higher investment in attractiveness is never for free, often being traded-off against reduced fertility (Figure 1). For example, there is a negative genetic correlation between sperm quality and colour ornaments in the guppy14 (Poecilia reticulata) and with courtship song in crickets15 (Teleogryllus oceanicus). Moreover, directional selection for increased comb size (in this case, the red fleshy crest on the male’s head) in the domestic chicken (Gallus domesticus) generated a correlated reallocation of resources away from  5 testes16. Worse follows, as the selective rationale of having larger sexual ornaments is to gain more matings. So given a limited budget, attractive males inevitably must divide their seminal resources into multiple, smaller ejaculates with likely reductions in their competitive fertility2,17.    These considerations make the explanation of Polak and colleagues6 based on enhanced sperm competition harder to swallow. A way out of this conundrum is that well-adorned males are simply of higher quality. It is an old and well-established idea that exaggerated sexual ornaments are condition-dependent handicap traits that signal male genetic and phenotypic quality18. High-quality males with larger sexual ornaments expect greater female interest and so they should suitably increase investment in reproductive traits, such as sperm or ejaculate proteins. Whether the imperative to service extra females results in more or less investment per ejaculate with sexual ornament size then depends on all the spice of life-history, such as the propensity of females to mate with several males (polyandry), her mate preference, male costs of sexual trait exaggeration, as well as the degree of sperm competition.   Ultimately, females also need to reap benefits from preferentially mating with ornamented males and will thus evolve to have reproductive tracts structured to favour particular ejaculate properties19. What Polak and colleagues6 have convincingly demonstrated is a positive genetic covariance between a sexual ornament and competitive fertilization success. These traits should be inherited, allowing dad's success to endow his[OK?] sons. If the condition-dependent hypothesis holds up, there are also associated ‘good genes’ for other aspects of male fitness to be passed on as well. We need to know a lot more about this before the whys and wherefores of D. bipectinata sex combs come fully into focus.     6 1. Sheldon, B. (1994). Male phenotype, fertility, and the pursuit of extra-pair copulations by female birds. Proc. R. Soc. B 257, 25-30.  2. Tazzyman, S. J., Pizzari, T., Seymour, R. M. and Pomiankowski, A. (2009). The evolution of continuous variation in ejaculate expenditure strategy. Am. Nat. 174, E71-E82.  3. Jones, T.M. (2001). A potential cost of monandry in the lekking sandfly Lutzomyia longipalpis. J. Insect Behav. 14, 385–399.   4. Preston, B.T., Stevenson, I.R., Pemberton, J.M. and Wilson, K. (2001). Dominant rams lose out by sperm depletion. Nature 409, 681–682.  5. Tazzyman, S. J., Seymour, R. M. and Pomiankowski, A. (2012). Fixed and dilutable benefits: female choice for good genes or fertility. Proc. R. Soc. B 279, 334-340.  6. Polak M., Hurtado-Gonzales J.L., Benoit J.B., Hooker K.J. and Tyler F. (2021). Positive genetic covariance between male sexual ornamentation and fertilizing capacity. Curr. Biol. 31, XXXXXXXXXX  7. Chapman, T., Bangham, J., Vinti, G., Seifried, B., Lung, O., Wolfner, M.F., Smith, H.K. and Partridge, L. (2003). The sex peptide of Drosophila melanogaster: female post-mating responses analyzed by using RNA interference. Proc. Natl. Acad. Sci. USA 100, 9923–28.  8. Wigby, S., Sirot, L.K., Linklater, J.R., Buehner, N., Calboli, F.C., Bretman, A., Wolfner, M.F. and Chapman, T. (2009). Seminal fluid protein allocation and male reproductive success. Curr. Biol. 19, 751–57.  9. Avila, F.W., Sirot, L.K., LaFlamme, B.A., Rubinstein, C.D., and Wolfner, M.F. (2011). Insect seminal fluid proteins: identification and function. Ann. Rev. Entomol. 56, 21-40.  10. Hosken, D.J., Garner, T.W.J. and Ward, P.I. (2001). Sexual conflict selects for male and female reproductive characters. Curr. Biol. 11, 489-493.  11. Parker, G.A. (2020). Conceptual developments in sperm competition: a very brief synopsis. Phil. Trans. R. Soc. B 375, 20200061. 12. Kustra, M.C. and Alonzo, S.H. (2020). Sperm and alternative reproductive tactics: a review of existing theory and empirical data. Phil. Trans. R. Soci. B 375, 20200075. 13. Simmons, L.W., Lupold, S. and Fitzpatrick, J.L. (2017). Evolutionary trade-off between secondary sexual traits and ejaculates. Trends Ecol. Evol. 32, 964-976.  14. Evans, J.P. (2010). Quantitative genetic evidence that males trade attractiveness for ejaculate quality in guppies. Proc. R. Soc. Lond. B 277, 3195–3202.  15. Simmons, L.W., Tinghitella, R.M. and Zuk, M. (2010). Quantitative genetic variation in courtship song and its covariation with immune function and sperm quality in the field cricket Teleogryllus oceanicus. Behav. Ecol. 21, 1330–1336. [AU et al after 10 authors]  7  16. von Schantz, T., Tufvesson, M., Göransson, G., Grahn, M., Wilhelmson, M. and Witzell, H. (1995). Artificial selection for increased comb size and its effects on other sexual characters and viability in Gallus domesticus (the domestic chicken). Heredity 75, 518–529. [AU et al after 10 authors]  17. Wedell, N., Gage, M. J. G. and Parker, G. A. (2002). Sperm competition, male prudence and sperm limited females. Trends Ecol. Evol. 17, 313-320.   18. Iwasa, Y. and Pomiankowski, A. (1999). Good parent and good gene models of handicap evolution. J. Theor. Biol. 200, 97-109.  19. Firman, R. C., Gasparini, C., Manier, M. K., and Pizzari, T. (2017). Postmating female control: 20 years of cryptic female choice. Trends Ecol. Evol. 32, 368–382.   20. Forstmeier, W., Ihle M., Opatová P., Martin K., Knief U., Albrechtová, J., Albrecht, T. and Kempenaers, B. (2017). Testing the phenotype-linked fertility hypothesis in the presence and absence of inbreeding. J. Evol. Biol. 30, 968-976. [AU et al after 10 authors]     8 Figure 1. Male sexual ornament associations with fertility.  During sexual engagement, male Drosophila bipectinata vibrate the sex combs on their tibia across the female's abdomen (top left; image: Michal Polak). Artificial selection6 reveals that the size of the sex comb is genetically correlated with a male's competitive fertilization success against a prior male's ejaculate (P2). A similar positive correlation between sexual ornaments and sperm traits associated with fertility has been found in the zebra finch, Taeniopygia guttata20 (center right). But contrary to this, Poecilia reticulata guppies (bottom right; image: Per Harald Olsen/Wkicommons) with more showy colours have slower swimming sperm14, males of the Australian cricket Teleogryllus oceanicus (bottom left; image: Nathan W. Bailey (CC BY 4.0)) which genetically produce longer song trills have fewer viable sperm in their ejaculates15 and domesticated chickens (top right; image: Francesco Veronesi (CC BY-SA 2.0) selected for larger head combs end-up with reduced testis size16. This mix of positive and negative  9 correlations reveal that investment trade-offs are likely to place limits on sexual ornament size as an indicator of a male's capability to succeed in sperm competition or to enhance female fertility.  

Sexual selection: Large sex combs signal male triumph in sperm competition

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Sexual selection: Large sex combs signal male triumph in sperm competition

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