A small writing assignment which is writing a critique of a scientific paper on Natural and Sexual Selection in Wild Insect Population Attachment includes the article The main guidelines for the crit

A small writing assignment which is writing a critique of a scientific paper on Natural and Sexual Selection in Wild Insect Population Attachment includes the article The main guidelines for the crit
Natural and Sexual Selection in a Wild Insect Population R. Rodríguez-Muñoz, 1A. Bretman, 1,2 J. Slate, 3C. A. Walling, 4T. Tregenza 1* The understanding of natural and sexual selection requires both field and laboratory studies to exploit the advantages and avoid the disadvantages of each approach. However, studies have tended to be polarized among the types of organisms studied, with vertebrates studied in the field and invertebrates in the lab. We used video monitoring combined with DNA profiling of all of the members of a wild population of field crickets across two generations to capture the factors predicting the reproductive success of males and females. The factors that predict a male ’s success in gaining mates differ from those that predict how many offspring he has. We confirm the fundamental prediction that males vary more in their reproductive success than females, and we find that females as well as males leave more offspring when they mate with more partners. I nsects are of fundamental importance to ter- restrial ecosystems but are underrepresented in studies that aim to understand how natural and sexual selection drive evolution in wild pop- ulations. Although poorly understood in their natural habitats, crickets have become an impor- tant laboratory model system, revealing complex forms of sexual selection whereby females choose between males according to their songs ( 1), males fight ( 2), females manipulate sperm from several males to favor unrelated males ( 3,4), and females lay eggs faster when mated to dominant males ( 2). However, although we now have many insights into the behavior and physiology of crickets in the laboratory, we have almost no idea how important these various aspects are in the insects ’natural habitat. This discrepancy is a cause for concern: Laboratory situations remove some sources of selection that may be very important in wild pop- ulations and may create new pressures; for in- stance, it may be that males that sing more get more mates in the lab, but in the field such males may die younger. Univoltine flightless field crickets, Gryllus campestris , hatch from eggs in early summer. Nymphs build burrows among the grass and spend the winter underground, emerging in spring to undergo one or two final molts to adulthood. Both sexes are highly territorial and spend the vast majority of their time in the immediate vicinity of a burrow entrance. A few days after becoming adults, males start to sing, and both males and females start moving frequently from one burrow to another in search of mates. To identify selec- tive pressures affecting behavior and to observe how behavior is correlated with fitness, we built a network of 64 motion-sens itive, infrared-equipped video cameras allowing us to monitor occupied burrows 24 hours a day throughout the breeding season. We tagged every newly emerged adult with a unique code to analyze their lives and be- haviors, including mating partners, how long par- ticular males and females spent together, the time that each male spent singing calling songs to at- tract females, and the fights that almost invariably occur when a male approaches a burrow occu- pied by another male. We used these fights to score males as either dominant or subordinate, reflect- ing the proportion of fights that he won ( 5). Al- though females never share burrows, they are only very rarely involved in aggressive interac- tions. Females visit or receive visits from neigh- boring males and frequently remain with a male for hours or days, sharing his burrow and mating repeatedly. From our videos, we inferred adult life span as the time from the observed emer- gence to the point when a cricket was either seen to be killed by a predator or was no longer found at any burrow. We observed that females began mating a few days after becoming adults and laid eggs directly into the ground throughout the breeding season (burrows are narrow, so molting and mating take place just outside and are easily observed). The crickets in the field in the second year of our ob- servations are therefore the offspring of the adults from the previous summer. Populations may ex- perience some migration, but this is likely to be very limited in our study population. The mead- ow is relatively isolated, being surrounded by little suitable habitat, and the observed immigra- tion rates of adults are low; therefore we had high success in assigning parentage within the popu- lation ( 5). All of these factors indicate that it is unlikely that substantial numbers of adult off- spring were missed because of emigration. Life- time reproductive success (LRS) was therefore inferred from the assignment of parentage from parents in 2006 to offspring in 2007 through the genotyping of all adults at 11 microsatellite loci. A key prediction of the theory of sexual se- lection (6 –8), assuming conventional sex roles and an even sex ratio, posits that males should have greater variance in LRS than females do. This prediction has been supported in a small number of studies of wild vertebrates [for exam- ple, ( 9)] and in laboratory experiments [although the lack of ecological context has led to debates over their relevance ( 10)]. Most studies of the cost and benefits of mates and matings in insects have been performed in the laboratory ( 11–13), and the only examination in the wild was of re- productive success estimated via the time female damselflies spent laying eggs after mating to a particular male ( 14). We directly examined both the number of mates that each individual had (controlling for differences in observational ef- fort) and the number of descendants they left in the next generation. The sex ratio was very close to even, which constrained the means to be the same for both sexes. As expected, we found that mean numbers of mates per day [males = 0.27 (0.40 SD), females = 0.25 (0.32 SD)] and of offspring sur- viving to adulthood [males = 1.92 (3.66 SD), fe- males = 1.79 (2.46 SD)] were, respectively, very similar. The small differences we observed were attributed to imperfections in observational data and in parentage assignment. The opportunity for selection can be estimated by comparing variances or coefficients of varia- tion ( 15). We examined with a randomization- 1Centre for Ecology and Conservation, School of Biosciences, University of Exeter, Cornwall Campus, Penryn TR10 EZ, UK. 2School of Biological Sciences, University of East Anglia, Norwich NR4 7TJ, UK. 3Department of Animal and Plant Sciences, University of Sheffie ld, Western Bank, Sheffield S10 2TN, UK. 4Institute of Evolutionary Biology, School of Bi- ological Sciences, Ashworth Lab oratories, King’s Buildings, University of Edinburgh, Edinburgh EH9 3JT, UK. *To whom correspondence should be addressed. E-mail: [email protected] Fig. 1. Number of adult offspring per individual. Frequencies for ( A) females and (B ) males. Males have significantly greater variance in offspring number relative to females. www.sciencemag.org SCIENCEVOL 328 4 JUNE 2010 1269 REPORTS on March 9, 2021 http://science.sciencemag.org/ Downloaded from based test (5) the prediction that males should show more variation than females, and we found no difference between the sexes in variance in the number of mates ( P= 0.39) but significantly more variance in the number of offspring produced by males (P = 0.033) (Fig. 1) ( 5). Similar results were found when controlling for the small dif- ferences in means between males and females (number of mates, P= 0.39; number of offspring, P = 0.028). It is, however, striking that although males varied more than females, the overall pat- terns were similar, with many females failing to leave any descendants. We found that both sexes benefit from mul- tiple mates. Females may use a single ejaculate over their reproductive lifetime, raising questions about why they mate with more than one male ( 16 ). Examination of traits expressed by both sexes indicated that individuals with a higher number of mates (standardized for monitoring effort) had a higher number of offspring for both male par- ents (Spearman ’srho=0.53, n= 47 individuals, P < 0.0001) and female parents (Spearman ’srho= 0.37, n= 55, P= 0.005). This suggests that the factors affecting the number of offspring produced by males are the same as those affecting the num- ber of offspring produced by females. Because there are numerous other correlations between traits, we also examined whether the number of mates was correlated with other behavioral and life- history traits by using a generalized linear model ( 5 ). This approach indicated that there were no interactions between sex and number of mates affecting LRS, nor any other significant interac- tions. Individuals of both sexes that were either larger, longer-lived, or had more mates had sig- nificantly higher LRS (analysis of deviance: size deviance = 4.58, F 1, 99 =4.58,P=0.035;longev- ity deviance = 117.14, F 1, 99 = 38.74,P< 0.0001; number of mates deviance = 44.47, F 1, 99 = 14.71, P = 0.0002) (Fig. 2). This demonstrates that not only do males increase their reproductive success through an increased number of mates, but females do better by mating with multiple partners, too. Al- though there is greater variance in male reproduc- tive success than in female reproductive success, this increased variance is not due to different effects of mate number between the sexes. Traits that confer success in gaining mates may differ from those that predict reproductive success because of differences among males in post-mating fertilization success and the viability of offspring ( 17). We counted the number of off- spring an individual had in the following gener- ation to measure directly the reproductive success of our field crickets. We found differences be- tween predictors of mating success and predictors of reproductive success. By comparing gener- alized linear models predicting mating success (measured as the number of females with which each male was observed to mate) with lifetime reproductive success (number of offspring sur- viving to adulthood), we identified factors that predicted the reproductive success of an individ- ual male. Mating success was predicted by domi- nance and an interaction between size and singing activity. Offspring number was also predicted by interactions between size and singing, but there was an additional interaction between longevity and singing and no significant effect of domi- nance. Contrary to expectations from lab studies that show that dominant males can monopolize mating access to females (18), who also prefer the odor of dominant males ( 19), we found that dom- inant males had fewer mates than did subordinate males (analysis of deviance: dominance deviance = 2.22, F 1, 24 = 9.58, P= 0.004) (Fig. 3A). This result is unexpected but reflects an ambiguous role for dominance in predicting mating success across species ( 20). For smaller males, the amount of singing was strongly correlated with the number of mates they obtained, whereas for larger males, singing activity was not associated with gaining more mates (size × singing deviance = 0.89, F 1, 23 =4.53, P= 0.044) (Fig. 3B). Similarly, for small males, singing effort affected the number of offspring (analysis of deviance: size × singing deviance = 25.93 F 1, 41 = 8.12, P= 0.007) (Fig. 3C). In ad- dition, short-lived males had more offspring when they sang more, whereas reproductive success in long-lived males was not dependent on a high rate of singing (longevity × singing deviance = 13.91, F 1, 41 =4.35, P= 0.043) (Fig. 3D). These interactions between naturally and sex- ually selected traits affecting different measures of reproductive success indicate that the benefits of sexually selected traits may vary according to other aspects of an individual ’s phenotype. The costs of sexually selected traits are expected to be lower in individuals of higher phenotypic condition, which in turn reflects the overall genetic quality ( 21 ). If males with high genetic quality are able to achieve a large size at adult emergence, they would be predicted to sing more. However, we observed no correlation between size and singing activity within males (Spearman ’s rho = 0.185, P =0.2, n= 47). Our results suggest that in this population, either size is not a reliable indicator of condition or male singing act ivity is not condition- dependent, despite its metabolic costs ( 22)and association with increased rates of parasitism ( 23) and predation ( 24). Size and singing activity are individually correlated with reproductive success, but the fact that smaller males benefit more from singing is the opposite of what we would expect if larger males are deemed to be those with the higher condition. This suggests that adult size is not an appropriate proxy for phenotypic condi- tion in these animals and possibly in other insects. Longevity is a fundamentally different trait from size, because it is not fixed at emergence to adulthood and hence can continue to be affected by other traits. The interaction between singing and longevity affecting reproductive success oc- curs because daily singing effort has a major ef- fect on offspring number in shorter-lived males Fig. 2. Determinants of male and female reproductive success measured as number of adult offspring in the following generation. Females are indicated by open symbols. ( A)Bodysize,( B) longevity (days), and ( C) number of mates per day. To aid in distinguishing data, where data points overlap, a small increment (0.02 to xand ycoordinates) has been added. Also, in (C), a number of points overlap at 0, 0 (16 males and 12 females) and would obscure further data, so have not received an increment. Larger body size, greater longevity, and a higher number of mates are inde- pendently associated with increased reproductive success in both males and females. 4 JUNE 2010 VOL 328 SCIENCEwww.sciencemag.org 1270 REPORTS on March 9, 2021 http://science.sciencemag.org/ Downloaded from but has no discernible effect in longer-lived males (Fig. 3D). This may be because if males live a long time, singing effort can be reduced once they have attracted a female to their burrow, whereas the population of short-lived males includes more individuals that are in poor condition and die young without mating or singing very much. In the laboratory, male crickets kept on a high-protein diet sang more, but lived for a shorter time (25). In the wild population, there was a strong positive correlation between daily singing effort and life span (Spearman’ s rho = 0.54,P< 0.0001, n= 47), most likely indicating that those that sang more were of higher quality. Our findings confirm the basic prediction that male reproductive success, while being constrained to be equal to that of females, is likely to vary more. Bateman’ sprediction(7) that this variation is due to the potentially higher mating rate of males does not appear to be borne out; variance in the number of mates a male had was no greater than that of females. Rather, it appears that in these insects, some males gain a disproportionately large share of the offspring in the following gen- eration through either greater success in postcopu- latory sexual selection or greater viability and survival of their offspring. Both sexes have higher LRSs when they have more mates, and there is no interaction between sex and number of mates that affects LRS. This demonstrates that polyandrous females have more offspring in the next generation, supporting pre- vious laboratory experiments (26). Because poly- androus females tend to have more matings as well as more mates, it is still unknown whether these benefits accrue from some direct source such as ejaculate compone nts or a need to replenish sperm stores, or whether they are the result of genetic benefits to the offspring of polyandrous females. It may be that polyandrous females can increase offspring fitness by preferentially fertil- izing their eggs with sperm from unrelated males ( 3 ) and that, by mating with multiple males, fe- males increase their chances of producing off- spring with unrelated males. The number of mates was a strong predictor of the number of descendants that both males and females left in the next generation. Similarly, traits associated with having several mates, such as male size and singing activity, were also asso- ciated with LRS, indicating that, in general, mating success is likely to perform quite well as a sur- rogate for overall reproductive success. However, it is clear that if we wish to understand selection on individual traits in natural populations, careful consideration must be given to how we measure reproductive success: Some traits that affected an individual ’s number of mates failed to predict LRS, and other traits associated with high LRS were not good predictors of mating success. Fur- thermore, interactions between naturally and sex- ually selected traits affecting both mating and reproductive success indicate that studying a sin- gle trait in isolation may be misleading. Our system bridges the divide between lab- oratory and field studies in evolutionary biology and indicates that, with the above caveats, con- clusions drawn from laboratory studies on crickets and, most likely, other insects as well are generally consistent with studies in the wild. We demon- strate here that the combination of video technol- ogy and genetic parentage assignment means that tracing reproductive success in wild invertebrates is no longer impractical and that we can now con- duct quantitative and functional genetic studies in natural populations. References and Notes1. M. Zuk, L. Simmons, in The Evolution of Mating Systems in Insects and Arachnids , J. C. Choe, B. J. Crespi, Eds. (Cambridge Univ. Press, Cambridge, 1997), pp. 89 –109. 2. A. Bretman, R. Rodríguez-Muñoz, T. Tregenza, Biol. Lett. 2 , 409 (2006). 3. A. Bretman, D. Newcombe, T. Tregenza, Mol. Ecol.18, 3340 (2009). 4. A. Bretman, N. Wedell, T. Tregenza, Proc. Biol. Sci.271, 159 (2004). 5. Supporting material is available on ScienceOnline. 6. C. R. Darwin, The Descent of Man and Selection in Relation to Sex ( John Murray, London, 1871). 7. A. J. Bateman, Heredity2, 349 (1948). 8. S. M. Shuster, M. J. Wade, Mating Systems and Strategies (Princeton Univ. Press, Princeton, NJ, 2003). 9. B. F. Snyder, P. A. Gowaty, Evolution61, 2457 (2007). 10. T. H. Clutton-Brock, Reproductive Success(Univ. of Chicago Press, Chicago, 1988). 11. T. Bilde, A. Foged, N. Schilling, G. Arnqvist, Science324, 1705 (2009). 12. T. Chapman, L. F. Liddle, J. M. Kalb, M. F. Wolfner, L. Partridge, Nature373, 241 (1995). 13. G. A. Schwarzenbach, D. J. Hosken, P. I. Ward, J. Evol. Biol. 18, 455 (2005). 14. O. M. Fincke, Evolution40, 791 (1986). 15. H. Kokko, A. Mackenzie, J. D. Reynolds, J. Lindström, W. J. Sutherland, Am. Nat.154, 358 (1999). 16. M. D. Jennions, M. Petrie, Biol. Rev. Camb. Philos. Soc. 75 , 21 (2000). 17. W. G. Eberhard, Female Control: Sexual Selection by Cryptic Female Choice (Princeton Univ. Press, Princeton, NJ, 1996). 18. N. Wedell, T. Tregenza, Evolution53, 620 (1999). 19. R.Kortet,A.Hedrick,Behav. Ecol. Sociobiol. 59,77 (2005). Fig. 3. Male sexual traits and mating and reproducti ve success. The effect on number of mates of ( A) dominance and (B ) the interaction between size and amount of singing, and the effect on number of adult offspring of ( C) the interaction between size and the amount of singing and ( D) the interaction between longevity and the amount o f singing. For illustrative purposes only, the 47 males were split into two groups by size (24 smaller and 23 larger males) or by longevity (24 shorter-lived and 23 longer-lived males). Open symbols and hatched lines indicate smaller [(B) and (C)] or shorter-lived (D) males. A number of data points overlap at 0, 0: nine smaller males and five larger in (B) and (C), and 14 short-lived males in (D). www.sciencemag.orgSCIENCEVOL 328 4 JUNE 2010 1271 REPORTS on March 9, 2021 http://science.sciencemag.org/ Downloaded from 20. A. Qvarnström, E. Forsgren,Trends Ecol. Evol.13, 498 (1998). 21. L. Rowe, D. Houle, Proc. Biol. Sci.263, 1415 (1996). 22. M. A. Hack, J. Insect Behav.11, 853 (1998). 23. M. Zuk, L. W. Simmons, L. Cupp, Behav. Ecol. Sociobiol. 33 , 339 (1993). 24. W. J. Bailey, S. Haythornthwaite, J. Zool. (London)244, 505 (1998). 25. J. Hunt et al.,Nature 432, 1024 (2004). 26. T. Tregenza, N. Wedell, Evolution52, 1726 (1998). 27. This work was supported by the Natural Environment Research Council (NERC) (grant NE/E005403/1), the NERC Sheffield Biomolecular Analysis Facility, the Leverhulme Trust, and a Royal Society Fellowship to T.T. We thank L. Rodríguez and M. C. Muñoz for providing access and facilities at the study site; J. M. López, C. López, E. González, C. R. del Valle, and F. González for assistance with the field work; and D. J. Hodgson and A. Wetherelt for assistance with data analysis and surveying. Supporting Online Materialwww.sciencemag.org/cgi/content/full/328/5983/1269/DC1 Materials and Methods Figs. S1 and S2 Table S1 References Movies S1 to S8 9 February 2010; accepted 12 April 2010 10.1126/science.1188102 Permissive Secondary Mutations Enable the Evolution of Influenza Oseltamivir Resistance Jesse D. Bloom, Lizhi Ian Gong, David Baltimore * The His 274→ Tyr 274 (H274Y) mutation confers oseltamivir resistance on N1 influenza neuraminidase but had long been thought to compromise viral fitness. However, beginning in 2007 –2008, viruses containing H274Y rapidly became predominant a mong human seasonal H1N1 isolates. We show that H274Y decreases the amount of neuraminidase that reaches the cell surface and that this defect can be counteracted by secondary mutations that also re store viral fitness. Two such mutations occurred in seasonal H1N1 shortly before the widespread appearance of H274Y. The evolution of oseltamivir resistance was therefore enabled by “permissive ”mutations that allowed the virus to tolerate subsequent occurrences of H274Y. An understanding of this process may provide a bas is for predicting the evolution of oseltamivir resistance in other influenza strains. I nfluenza A is a respiratory virus that causes annual epidemics and occasional pandemics, of which the worst on record killed in excess of 20 million people worldwide ( 1). One of the main defenses against influenza is the antiviral drug oseltamivir (Tamiflu, F. Hoffmann-La Roche, Incorporated) ( 2), and over 200 million doses have been stockpiled worldwide ( 3). Oseltamivir binds in the active site of the neuraminidase (NA) enzyme expressed on the virion surface, preventing it from cleaving sialic acid moieties that can be bound by the viral hemagglutinin protein ( 2). This lack of NA activity inhibits the release of newly formed virions from infected cells ( 4), as well as causing viral aggregation ( 4), reducing infectivity ( 5, 6), and limiting the ability of viruses to penetrate mucus found in the airways ( 6). During clinical testing of oseltamivir, a small fraction of human participants who were infected with the seasonal human H1N1 influenza strain A/Texas/36/1991 (TX91) and then treated with oseltamivir eventually shed resistant viruses ( 7). These viruses carried a mutation of histidine to tyrosine at NA residue 274 (H274Y), which is found near but not directly in the substrate- binding pocket ( 8). This mutation causes subtle structural alterations that weaken oseltamivir binding (8 ,9). However, TX91 viruses with H274Y were attenuated in tissue culture, mice, and fer- rets ( 10). H274Y also impaired the growth of the H1N1labstrainA/WSN/33(WSN)intissuecul- ture (11 ) and the infectivity of the seasonal H1N1 strain A/New Caledonia/20/1999 (NC99) in fer- rets (12 ). These studies led to the conclusion that “ [v]irus carrying a H274Y mutation is unlikely to be of clinical consequence ( 10).” This conclusion held sway from the intro- duction of oseltamivir as a drug in 1999 until the 2007– 2008 influenza season, when oseltamivir- Division of Biology, California Institute of Technology, Pas- adena, CA 91125, USA. *To whom correspondence should be addressed. E-mail: [email protected] Fig. 1. H274Y decreases NA surface expression and viral fitness for H1N1 lab strains. (A ) Plasmids encoding wild-type (WT, bla ck squares) or H274Y (gray circles) NAs were transfected into 293T cells. Cell s were assayed for total surface NA activity in a nonlysing buffer. (B ) The same cells were assayed by flow cytometry for mean surface NA expression using a monoclonal antibody against the PR8 tetramer. (C) Surface activity of WT, H274Y, or H274Y-R194G WSN NA at 18 hours. All four graphs show mean TSEM for at least three independent transfections. ( D) An estimated 50 infectious particles of each color of WSN-PB1flank-eGFP and/or mCherry carrying the indicated NA mutations were infected into 2.5 × 10 5A549-CMV-PB1 cells. After 46 to 50 hours, th e cells were analyzed by flow cytometry to quantify virus growth. Numbers give percentages of cells in ea ch gate; one representative plot is shown for each virus pair. (E) Relative fitness (ratio of Malthusian growth parameters) with respect to WT calculated from at least e ight replicates. Shown are geometricmeans and 95% confidence intervals. 4 JUNE 2010 VOL 328 SCIENCEwww.sciencemag.org 1272 REPORTS on March 9, 2021 http://science.sciencemag.org/ Downloaded from Natural and Sexual Selection in a Wild Insect Population R. Rodríguez-Muñoz, A. Bretman, J. Slate, C. A. Walling and T. Tre genza DOI: 10.1126/science.1188102 (5983), 1269-1272. 328 Science  reproductive success varies more than that of females. crickets. Adding genetic data allowed evaluation of how behavior impacts reproductive success and confirmed that male by comprehensively monitoring the life histories, behavior, and reproduc tive success of an entire population of field ) bridge this gap Zuk (p. 1269; see the Perspective by et al. Rodríguez-Muñoz the lab versus the natural environment. populations have often neglected invertebrates, resulting in a chasm bet ween our understandings of how things work in study of physiology and genetics. Studies examining how natural and sexu al selection operate to drive evolution in wild Insects are of fundamental importance to terrestrial ecosystems and prov ide laboratory model systems for the Insects in the Wild ARTICLE TOOLS http://science.sciencemag.org/content/328/5983/1269 MATERIALS SUPPLEMENTARY http://science.sciencemag.org/content/suppl/2010/06/03/328.5983.1269.DC2 http://science.sciencemag.org/content/suppl/2010/06/02/328.5983.1269.DC1 CONTENT RELATED http://science.sciencemag.org/content/sci/328/5983/1298.2.full http://science.sciencemag.org/content/sci/328/5983/1237.full REFERENCES http://science.sciencemag.org/content/328/5983/1269#BIBL This article cites 20 articles, 1 of which you can access for free PERMISSIONS http://www.sciencemag.org/help/reprints-and-permissions Terms of Service Use of this article is subject to the is a registered trademark of AAAS. Science Science, 1200 New York Avenue NW, Washington, DC 20005. The title (print ISSN 0036-8075; online ISSN 1095-9203) is published by the Amer ican Association for the Advancement of Science Copyright © 2010, American Association for the Advancement of Science on March 9, 2021 http://science.sciencemag.org/ Downloaded from