scholarly journals The growth factor BMP11 is required for the development and evolution of a male exaggerated weapon and its associated fighting behavior in a water strider

PLoS Biology ◽  
2021 ◽  
Vol 19 (5) ◽  
pp. e3001157
Author(s):  
William Toubiana ◽  
David Armisén ◽  
Séverine Viala ◽  
Amélie Decaras ◽  
Abderrahman Khila

Exaggerated sexually selected traits, often carried by males, are characterized by the evolution of hyperallometry, resulting in their disproportionate growth relative to the rest of the body among individuals of the same population. While the evolution of allometry has attracted much attention for centuries, our understanding of the developmental genetic mechanisms underlying its emergence remains fragmented. Here we conduct comparative transcriptomics of the legs followed by an RNA interference (RNAi) screen to identify genes that play a role in the hyperallometric growth of the third legs in the males of the water strider Microvelia longipes. We demonstrate that a broadly expressed growth factor, Bone Morphogenetic Protein 11 (BMP11, also known as Growth Differentiation Factor 11), regulates leg allometries through increasing the allometric slope and mean body size in males. In contrast, BMP11 RNAi reduced mean body size but did not affect slope either in the females of M. longipes or in the males and females of other closely related Microvelia species. Furthermore, our data show that a tissue-specific factor, Ultrabithorax (Ubx), increases intercept without affecting mean body size. This indicates a genetic correlation between mean body size and variation in allometric slope, but not intercept. Strikingly, males treated with BMP11 RNAi exhibited a severe reduction in fighting frequency compared to both controls and Ubx RNAi-treated males. Therefore, male body size, the exaggerated weapon, and the intense fighting behavior associated with it are genetically correlated in M. longipes. Our results support a possible role of pleiotropy in the evolution of allometric slope.

2020 ◽  
Author(s):  
William Toubiana ◽  
David Armisén ◽  
Decaras Amélie ◽  
Abderrahman Khila

AbstractExaggerated sexually selected traits, often carried by males, are characterized by the evolution of hyperallometry, resulting in their disproportionate growth relative to the rest of the body 1–3. While the evolution of allometry has attracted much attention for centuries, our understanding of the developmental genetic mechanisms underlying its emergence remains fragmented 4,5. Here we show that the hyperallometric legs in the males of the water strider Microvelia longipes are associated with a specific signature of gene expression during development. Using RNAi knockdown, we demonstrate that a broadly expressed growth factor, Bone Morphogenetic Protein 11 (BMP11, also known as Growth Differentiation Factor 11), regulates leg allometries through increasing the allometric coefficient and mean body size in males. In contrast, BMP11 RNAi reduced mean body size but did not affect slope in females. Furthermore, our data show that a tissue specific factor, Ultrabithorax (Ubx), increases intercept without affecting mean body size. This indicates a genetic correlation between mean body size and variation in allometric slope, but not intercept. Strikingly, males treated with BMP11 RNAi exhibited a severe reduction in fighting frequency compared to both controls and Ubx RNAi-treated males. Overall, we demonstrate a genetic correlation between male body size, the exaggerated weapon, and the intense fighting behaviour associated with it in M. longipes. Our results provide evidence for a role of pleiotropy in the evolution of allometric slope.


Author(s):  
Jason W Millington ◽  
George P Brownrigg ◽  
Paige J Basner-Collins ◽  
Ziwei Sun ◽  
Elizabeth J Rideout

Abstract In Drosophila raised in nutrient-rich conditions female body size is approximately 30% larger than male body size due to an increased rate of growth and differential weight loss during the larval period. While the mechanisms that control this sex difference in body size remain incompletely understood, recent studies suggest that the insulin/insulin-like growth factor signaling pathway (IIS) plays a role in the sex-specific regulation of processes that influence body size during development. In larvae, IIS activity differs between the sexes, and there is evidence of sex-specific regulation of IIS ligands. Yet, we lack knowledge of how changes to IIS activity impact body size in each sex, as the majority of studies on IIS and body size use single- or mixed-sex groups of larvae and/or adult flies. The goal of our current study was to clarify the body size requirement for IIS activity in each sex. To achieve this goal we used established genetic approaches to enhance, or inhibit, IIS activity, and quantified pupal size in males and females. Overall, genotypes that inhibited IIS activity caused a female-biased decrease in body size, whereas genotypes that augmented IIS activity caused a male-specific increase in body size. This data extends our current understanding of body size regulation by showing that most changes to IIS pathway activity have sex-biased effects, and highlights the importance of analyzing body size data according to sex.


2014 ◽  
Vol 10 (3) ◽  
pp. 20130869 ◽  
Author(s):  
J. F. Lemaître ◽  
C. Vanpé ◽  
F. Plard ◽  
J. M. Gaillard

Allometric relationships between sexually selected traits and body size have been extensively studied in recent decades. While sexually selected traits generally display positive allometry, a few recent reports have suggested that allometric relationships are not always linear. In male cervids, having both long antlers and large size provides benefits in terms of increased mating success. However, such attributes are costly to grow and maintain, and these costs might constrain antler length from increasing at the same rate as body mass in larger species if the quantity of energy that males can extract from their environment is limiting. We tested for possible nonlinearity in the relationship between antler size and body mass (on a log–log scale) among 31 cervids and found clear deviation from linearity in the allometry of antler length. Antler length increased linearly until a male body mass threshold at approximately 110 kg. Beyond this threshold, antler length did not change with increasing mass. We discuss this evidence of nonlinear allometry in the light of life-history theory and stress the importance of testing for nonlinearity when studying allometric relationships.


Mammalia ◽  
2017 ◽  
Vol 81 (2) ◽  
Author(s):  
Luíza Z. Magnus ◽  
Nilton Cáceres

AbstractTribosphenic molars are considered great innovations in mammals and are related to several structures and variables that can explain adaptation. The aim of this study was to investigate the importance of body size and habitat relation, using a phylogenetic approach, in the first lower molar shape in didelphid marsupials. Geometric morphometric analyses of the lower molar’s shape were performed on 261 specimens, 130 females and 131 males, covering 14 genera and 37 species of the Didelphidae family. The molar conformation showed a larger talonid in relation to the trigonid in more arboreal genera, and narrower and longer molars in genera with a larger body size. Phylogeny was the variable with the highest explanation for both females and males (16.17% and 9.02%, respectively). The body size was significant in males, presenting an important influence on molar shape, while the body size in females was not significant when phylogenetic relationship was controlled for. In both sexes, habitat presents a strong effect of phylogeny, with no direct effect on molar shape. Didelphid molar shape is another result of its phylogenetic history and does not respond very much to environmental pressures. Male body size influences molar shape in didelphids, even in the presence of a strong phylogenetic signal.


Behaviour ◽  
2004 ◽  
Vol 141 (3) ◽  
pp. 327-341 ◽  
Author(s):  
Wolf Blanckenhorn ◽  
Claudia Mühlhäuser

AbstractIn the common dung or black scavenger fly Sepsis cynipsea (Diptera: Sepsidae) several morphological and behavioural male and female traits interact during mating. Previous studies show that males attempt to mount females without courtship, females use vigorous shaking behaviour in response to male mounting, the duration of shaking is an indicator of both direct and indirect female choice and sexual conflict, and larger males enjoy a mating advantage. We conducted a quantitative genetic paternal half sib study to investigate the genetic underpinnings of these traits, notably body size (the preferred trait) and the associated female preference, and to assess the relative importance of various models generally proposed to account for the evolution of sexually selected traits. Several morphological traits and female shaking duration were heritable, thus meeting a key requirement of all sexual selection models. In contrast, two traits indicative of male persistence in mating were not. Male longevity was also heritable and negatively correlated with his mating effort, suggesting a mating cost. However, the crucial genetic correlation between male body size and female shaking duration, predicted to be negative by both 'good genes' and Fisherian models and positive by the sexual conflict (or chase-away) model, was zero. This could be because of low power, or because of constraints imposed by the genetic correlation structure. Based on our rsults we conclude that discriminating sexual selection models by sole means of quantitative genetics is difficult, if not impossible.


2020 ◽  
Author(s):  
Jason W. Millington ◽  
George P. Brownrigg ◽  
Paige J. Basner-Collins ◽  
Ziwei Sun ◽  
Elizabeth J. Rideout

ABSTRACTIn Drosophila, female body size is approximately 30% larger than male body size due to an increased rate of larval growth. While the mechanisms that control this sex difference in body size remain incompletely understood, recent studies suggest that the insulin/insulin-like growth factor signaling pathway (IIS) plays a role in the sex-specific regulation of growth during development. In larvae, IIS activity differs between the sexes, and there is evidence of sex-specific regulation of IIS ligands. Yet, we lack knowledge of how changes to IIS activity impact growth in each sex, as the majority of studies on IIS and body size use single- or mixed-sex groups of larvae and/or adult flies. The goal of our current study was to clarify the requirement for IIS activity in each sex during the larval growth period. To achieve this goal we used established genetic approaches to enhance, or inhibit, IIS activity, and quantified body size in male and female larvae. Overall, genotypes that inhibited IIS activity caused a female-biased decrease in body size, whereas genotypes that augmented IIS activity caused a male-specific increase in body size. This data extends our current understanding of larval growth by showing that most changes to IIS pathway activity have sex-biased effects on body size, and highlights the importance of analyzing data by sex in larval growth studies.


2016 ◽  
Vol 12 (2) ◽  
pp. 20150957 ◽  
Author(s):  
Alissa G. Anderson ◽  
Eileen A. Hebets

In sexually cannibalistic animals, male fitness is influenced not only by successful mate acquisition and egg fertilization, but also by avoiding being eaten. In the cannibalistic nursery web spider, Pisaurina mira , the legs of mature males are longer in relation to their body size than those of females, and males use these legs to aid in wrapping a female's legs with silk prior to and during copulation. We hypothesized that elongated male legs and silk wrapping provide benefits to males, in part through a reduced likelihood of sexual cannibalism. To test this, we paired females of random size with males from one of two treatment groups—those capable of silk wrapping versus those incapable of silk wrapping. We found that males with relatively longer legs and larger body size were more likely to mate and were less likely to be cannibalized prior to copulation. Regardless of relative size, males capable of silk wrapping were less likely to be cannibalized during or following copulation and had more opportunities for sperm transfer (i.e. pedipalpal insertions). Our results suggest that male size and copulatory silk wrapping are sexually selected traits benefiting male reproductive success.


2015 ◽  
Vol 370 (1673) ◽  
pp. 20140220 ◽  
Author(s):  
Amy M. Boddy ◽  
Hanna Kokko ◽  
Felix Breden ◽  
Gerald S. Wilkinson ◽  
C. Athena Aktipis

The factors influencing cancer susceptibility and why it varies across species are major open questions in the field of cancer biology. One underexplored source of variation in cancer susceptibility may arise from trade-offs between reproductive competitiveness (e.g. sexually selected traits, earlier reproduction and higher fertility) and cancer defence. We build a model that contrasts the probabilistic onset of cancer with other, extrinsic causes of mortality and use it to predict that intense reproductive competition will lower cancer defences and increase cancer incidence. We explore the trade-off between cancer defences and intraspecific competition across different extrinsic mortality conditions and different levels of trade-off intensity, and find the largest effect of competition on cancer in species where low extrinsic mortality combines with strong trade-offs. In such species, selection to delay cancer and selection to outcompete conspecifics are both strong, and the latter conflicts with the former. We discuss evidence for the assumed trade-off between reproductive competitiveness and cancer susceptibility. Sexually selected traits such as ornaments or large body size require high levels of cell proliferation and appear to be associated with greater cancer susceptibility. Similar associations exist for female traits such as continuous egg-laying in domestic hens and earlier reproductive maturity. Trade-offs between reproduction and cancer defences may be instantiated by a variety of mechanisms, including higher levels of growth factors and hormones, less efficient cell-cycle control and less DNA repair, or simply a larger number of cell divisions (relevant when reproductive success requires large body size or rapid reproductive cycles). These mechanisms can affect intra- and interspecific variation in cancer susceptibility arising from rapid cell proliferation during reproductive maturation, intrasexual competition and reproduction.


2019 ◽  
Vol 59 (5) ◽  
pp. 1290-1302 ◽  
Author(s):  
Rafael Lucas Rodríguez ◽  
William G Eberhard

AbstractSexually-selected traits often show positive static allometry, with large individuals bearing disproportionately large structures. But many other sexually-selected traits show isometry or even negative allometry, with trait size varying relatively little with body size. We recently proposed that the functions of these traits (as aggressive signals, weapons, courtship signals, and contact courtship devices) determine their allometries. Positive allometry is generally favored for aggressive signals because aggressive signals are selected to emphasize body size (and thus fighting prowess). In contrast, the biomechanics of force application in weapons only sometimes select for positive allometry; the content of courtship signals is even less often related to body size; and contact courtship devices are selected to be relatively invariant across body sizes. Here we summarize the arguments in favor of this “functional allometry” hypothesis and expand a comparative test of its predictions. Our results indicate that sexual traits have the allometric slopes predicted by our hypothesis, regardless of which body part bears the structure.


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