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Trade‐offs during the Development of Primary and Secondary Sexual Traits in a Horned Beetle
Abstract
Resource allocation trade-offs during development affect the final sizes of adult structures and have the potential to constrain the types and magnitude of evolutionary change that developmental processes can accommodate. Such trade-offs can arise when two or more body parts compete for a limited pool of resources to sustain their growth and differentiation. Recent studies on several holometabolous insects suggest that resource allocation trade-offs may be most pronounced in tissues that grow physically close to each other. Here we examine the nature and magnitude of developmental trade-offs between two very distant body parts: head horns and genitalia of males of the horned scarab beetle Onthophagus taurus. Both structures develop from imaginal disklike tissues that undergo explosive growth during late larval development but differ in exactly when they initiate their growth. We experimentally ablated the precursor cells that normally give rise to male genitalia at several time points during late larval development and examined the degree of horn development in these males compared to that of untreated and sham-operated control males. We found that experimental males developed disproportionately larger horns. Horn overexpression was weakest in response to early ablation and most pronounced in males whose genital disks were ablated just before larvae entered the prepupal stage. Our results suggest that even distant body parts may rely on a common resource pool to sustain their growth and that the relative timing of growth may play an important role in determining whether, and how severely, growing organs will affect each other during development. We use our findings to discuss the physiological causes and evolutionary consequences of resource allocation trade-offs.
... In a study where testis size is measured and sperm are counted [19], the male larvae exposed to larval cues, regardless of sex, produce smaller testes but more fertile sperm. These discoveries suggest that in response to their social environment, male larvae are able to dedicate varying portions of testis volumes to spermatogenesis and other functions [41], resulting in potential trade-offs between traits of different functions [19,[42][43][44]. However, there is no report that insects can alter their testis size in response to the socio-sexual environment experienced at the adult stage. ...
... However, there is no report that insects can alter their testis size in response to the socio-sexual environment experienced at the adult stage. This may be because most resource allocation to traits making up the adult body takes place during growth and development [42,43,[45][46][47][48], leaving little room for adults to change their testis morphology. To date, it is not clear whether insect pupae can alter their testis size after exposure to different socio-sexual environments. ...
... The above diverse responses to social cues may be attributed to the fact that resource allocation to morphological traits and spermatogenesis takes place in different life stages. Evidence shows that most adult morphological traits are formed during the larval stage [42,43,47,48], allowing the larvae but not pupae and adults to adjust their testis size. Lepidopteran males produce most eupyrene sperm during the larval and pupal stages, most apyrene sperm during the pupal stage [53] and continue to produce both types of sperm during the adult stage [10]. ...
Theoretic and empirical studies show that social surroundings experienced by male insects during their larval or adult stage can influence their testicular investment in diverse ways. Although insect pupae do not feed and crawl, they can communicate using sex-specific and/or non-sex specific cues. Yet, it is unknown, in any insect, whether and how male pupae can fine-tune their resource allocation to sperm production and testis size in response to socio-sexual environments. We investigated this question using a moth, Ephestia kuehniella, which produces fertile eupyrene sperm and unfertile apyrene sperm. We held male pupae individually or in groups with different sex ratios, and dissected adults upon eclosion, measured their testis size, and counted both types of sperm. We demonstrated that after exposure to conspecific pupal cues regardless of sex, male pupae increased production of eupyrenes and apyrenes at the same rate but kept testis size unchanged. We suggest that testis size is fixed after pupation because most morphological traits are formed during the larval stage, allowing little room for pupae to adjust testis size. Like adults, male pupae with fully grown testes have sufficient resources to produce more sperm of both types according to the perceived increase in sperm competition risk.
... In a study where testis size is measured and sperm are counted [19], the male larvae exposed to larval cues regardless of sex produce smaller testes but more fertile sperm. These discoveries suggest that in response to their social environment, male larvae are able to dedicate varying portions of testis volumes to spermatogenesis and other functions [41], resulting in potential trade-offs between traits of different functions [19,[42][43][44]. However, there is no report that insect adults can alter their testis size in response to the socio-sexual environment. ...
... However, there is no report that insect adults can alter their testis size in response to the socio-sexual environment. This may be because most resource allocation to traits making up the adult body takes place during growth and development [42,43,[45][46][47][48], leaving little room for adults to change their testis morphology. To date, it is not clear whether insect pupae can alter their testis size after exposure to different socio-sexual environments. ...
... Evidence shows that most adult morphological traits are formed during the larval stage [42,43,47,48], allowing the larvae but not pupae and adults to adjust their testis size. Lepidopteran males produce most eupyrene sperm during the larval and pupal stages, most apyrene sperm during the pupal stage [53] and continue to produce both types of sperm during the adult stage [10]. ...
Theoretic and empirical studies show that social surroundings experienced by male insects during their larval or adult stage can influence their testicular investment in diverse ways. Although insect pupae do not feed and crawl, they can communicate using sex-specific and/or non-sex specific cues. Yet, it is unknown, in any insect, whether and how male pupae can fine-tune their resource allocation to sperm production and testis size in response to socio-sexual environment. We investigated this question using a moth, Ephestia kuehniella, which produces fertile eupyrene sperm and unfertile apyrene sperm. We held male pupae individually or in groups with different sex ratios, and dissected adults upon eclosion, measured their testis size, and counted both types of sperm. We demonstrated that after exposure to conspecific pupal cues regardless of sex, male pupae increased production of eupyrenes and apyrenes at the same rate but kept testis size unchanged. We suggest that testis size is fixed after pupation because most morphological traits are formed during the larval stage, allowing little room for pupae to adjust testis size. Like adults, male pupae with fully grown testes have sufficient resources to produce more sperm of both types according to the perceived increase of sperm competition risk.
... Although hierarchical models can be a useful heuristic, they might also be misleading because much remains unknown about the nature of allocation and investment. For example, trait proximity, tissue expense and developmental timing can influence trait investment, leading to trade-offs that are not purely based on functional grouping [16][17][18][19][20][21]. Our lack of knowledge on the principles that govern resource allocation and investment is a critical obstacle in our understanding of reproductive trait evolution. ...
... Male-female comparisons have been useful throughout the history of biology [22][23][24]. However, until now, studies of trade-offs in pre-and post-copulatory sexual traits have focused predominately on males [6,19,[25][26][27]. The extent to which homologues in females follow similar allocation patterns is relatively unknown. ...
... Developmental timing is another factor hypothesized to play a role in the presence and magnitude of trade-offs [20,21]. For example, Moczek & Nijhout [19] discovered that testes ablation in male beetles led to horn growth in medium-sized individuals, but only when those testes were ablated during the period of horn growth. Males of this size did not grow sizeable horns if ablation occurred earlier in development. ...
Sexually selected weapons are assumed to trade off with traits related to ejaculates, such as testes. However, remarkably little is known about what governs resource allocation and why trade-offs are found in some cases and not others. Often-used models depict competitive allocation occurring within the functional grouping of traits (e.g. reproduction); however, other factors including tissue expense and developmental timing may influence allocation. Experimental comparisons of investment across the sexes have the potential to illuminate allocation rules, because the sexes do not always use traits for the same functions. Here, we capitalize upon a species where females have weapons-testes homologues. We report that a documented trade-off in investment between hind-limb weapons and testes in leaf-footed cactus bugs, Narnia femorata, is even more pronounced in female hind limbs and ovaries. Female hind limbs in this species do not share the clear reproductive function of male hind limbs; therefore, this trade-off spans trait functional groups. Such patterns of investment suggest that future studies of reproductive trade-offs should consider factors such as tissue expense and developmental timing.
... In another study, researchers examined potential developmental trade-offs between head horns, a sexually-selected trait, and genitalia of male horned scarab beetles (Onthophagus taurus; Moczek and Nijhout, 2004). Their experiment involved removing the genital precursor tissues, referred to as disks, during development to test for impacts on horn growth. ...
... Interestingly, one of the hypotheses these authors sought to test was whether structures located at opposite ends of the body, rather than those situated adjacent or very close, would be seen to compete for resources. They concluded that structures draw from the same resource pool and will thus compete for those resources, irrespective of their specific location on the body (Moczek and Nijhout, 2004). ...
... Prior evidence where brain and body tissues were directly measured largely comes from nonhuman animals (e.g. Moczek and Nijhout, 2004;Isler and van Schaik, 2006;Navarette et al., 2011;Kotrschal et al., 2013). Studies which have found evidence for tissue competition in humans have mostly done so using proxies for the brain, visceral organs or skeletal muscle size, such as head, abdominal and arm circumferences (e.g. ...
The ‘expensive-tissue’ hypothesis of Aiello and Wheeler is well-known in anthropology for positing that an increasingly small gut was a key factor in the evolution of the large hominin brain. The insight that organs and tissues in the body compete for energy resources was also central to the ‘thrifty phenotype’ hypothesis of Hales and Barker, which proposed that nutritional stress in fetal life resulted in differential growth of the brain and pancreas. Both hypotheses are consistent with life history theory, which assumes that energy allocation trade-offs occur in energylimited environments. The prediction that somatic traits trade off against one another in the context of the body’s fixed energy budget has, however, yet to be rigorously tested in humans. The current thesis project aimed to fill this gap by recruiting 70 healthy young women and obtaining comprehensive, high-quality data on their brain and body composition. This included, specifically, measures of brain gray and white matter volume, fat mass, skeletal muscle mass, and volumes of the heart, liver, kidneys and spleen. Additional outcomes included resting energy expenditure and two proxies of early-life growth: birth weight, a marker of fetal weight gain, and tibia length, a marker of linear growth indexing postnatal experience. With these data, three principal hypotheses were tested: 1) there is variation in the energy expenditure of tissues and organs; 2) trade-offs are observed between brain and body organs/tissues; and 3) trade-off relationships are mediated by early-life growth. Results suggest the metabolic cost of organs and tissues is variable, and that the brain – in particular its gray matter component – trades off against lean tissues in the body (i.e. skeletal muscle, the liver and kidneys), but not fat mass. However, less support was found for the prediction that trade-offs are mediated by fetal and infant growth.
... Larger, sturdier weapons are predicted to allow males to better compete for high-quality territories and mating opportunities, likely increasing reproductive success (Miyatake 1997;Eberhard 1998;Kelly 2008;Yamane et al. 2010;McCullough et al. 2016). However, many weapons are costly to produce and maintain (Emlen 2001;Allen and Levinton 2007; but see McCullough and Emlen 2013;McCullough and Tobalske 2013) and can compete for a limited supply of resources within an individual (Nijhout and Emlen 1998;Moczek and Nijhout 2004;Tomkins et al. 2005). Therefore, an individual that grows larger weapons is predicted to have fewer resources available to invest in other bodily structures (Kawano 1997;Tomkins et al. 2005;Yamane et al. 2010). ...
... Studies incorporating phenotypic engineering can provide powerful experimental complements to existing research, allowing a level of inference that cannot be achieved through observational studies alone (Zera and Harshman 2001;Simmons et al. 2017). Though few in number, experiments that have manipulated weapon growth (Fry 2006;Simmons and Emlen 2006) and testes growth (Moczek and Nijhout 2004) support a weapons-testes trade off ). However many phenotypic engineering studies use ablation methods, via micro-cauterization, which administer unnatural trauma to study subjects. ...
... It is important to note that N. femorata is a hemimetabolous insect; as such, adult structures develop slowly as juveniles continue to acquire food from their environment. Thus, these results challenge the idea that morphological tradeoffs might be limited to closed systems, such as the pupae of holometabolous species (Moczek and Nijhout 2004;Tomkins et al. 2005). In a study conducted shortly after this one, Somjee et al. (2017) found evidence of a similar weapons-testes trade-off in another hemimetabolous insect in the same family (Coreidae). ...
Costly sexually selected weapons are predicted to trade off with postcopulatory traits, such as testes. Although weapons can be important for achieving access to females, individuals of some species can permanently drop (i.e. autotomize) their weapons, without regeneration, to escape danger. We capitalized on this natural behavior to experimentally address whether the loss of a sexually selected weapon leads to increased testes investment in the leaf-footed cactus bug, Narnia femorata Stål (Hemiptera: Coreidae). In a second experiment, we measured offspring production for males that lost a weapon during development. As predicted, males that dropped a hind limb during development grew significantly larger testes than the control treatments. Hind-limb autotomy did not result in the enlargement of other nearby traits. Our results are the first to experimentally demonstrate that males compensate for natural weapon loss by investing more in testes. In a second experiment we found that females paired with males that lost a hind limb had 40% lower egg hatching success than females paired with intact males, perhaps because of lower mating receptivity to males with a lost limb. Importantly, in those cases where viable offspring were produced, males missing a hind limb produced 42% more offspring than males with intact limbs. These results suggest that the loss of a hind-limb weapon can, in some cases, lead to greater fertilization success.
... Consistent with this prediction, interspecific comparisons across several taxa have revealed that traits subject to precopulatory selection, such as weaponry and body size, often correlate negatively with traits subject to postcopulatory selection, such as testis size (Heske and Ostfeld 1990;Poulin and Morand 2000;Fitzpatrick et al. 2012;Dines et al. 2015;Dunn et al. 2015). In addition to the potential role of precopulatory selection in limiting the opportunity for postcopulatory selection, such negative interspecific correlations could also arise from (or be strengthened by) energetic trade-offs between sexually selected traits (Moczek and Nijhout 2004;Simmons and Emlen 2006;Kelly 2008;Parker and Pizzari 2010;Yamane et al. 2010;Somjee et al. 2015). However, analyses in other taxa have found no evidence for negative interspecific correlations between targets of pre-and postcopulatory selection (Ferrandiz-Rovira et al. 2014;L€ upold et al. 2014), and several studies have documented positive correlations (Wedell 1993;L€ upold et al. 2014). ...
... Notably, the negative correlations that we observed have regression and correlation coefficients near the high end of those reported for most other lineages (Poulin and Morand 2000;Fitzpatrick et al. 2012;L€ upold et al. 2014;Dines et al. 2015). These negative interspecific correlations mirror the trade-off between body size (or weaponry) and relative testis size that is often observed within species (Moczek and Nijhout 2004;Simmons and Emlen 2006;Kelly 2008;Parker and Pizzari 2010;Yamane et al. 2010;Somjee et al. 2015). However, our results stand in contrast to other comparative studies that have documented non-significant or even positive interspecific correlations between the targets of pre-and postcopulatory sexual selection in bushcrickets (Wedell 1993), ungulates (Ferrandiz-Rovira et al. 2014L€ upold et al. 2014), and a Figure 1. ...
... As such, the tendency for SSD and testis size to covary negatively despite the presumably imperfect relationship between the strength of pre-and postcopulatory selection suggests that proximate energetic constraints on the expression of these traits may further help to structure the negative relationships that we observed. When precopulatory selection is strong, males typically allocate more resources to body size and weaponry, whereas in species where postcopulatory selection is strong, males often invest primarily in traits that improve their success in sperm competition (Moczek and Nijhout 2004;Simmons and Emlen 2006;Kelly 2008;Parker and Pizzari 2010;Yamane et al. 2010;Somjee et al. 2015). Evidence for the latter is limited in squamates, although sperm production is energetically costly in snakes and lizards (Olsson et al. 1997;Kahrl and Cox 2015). ...
Sexual selection reflects the joint contributions of precopulatory selection, which arises from variance in mating success, and postcopulatory selection, which arises from variance in fertilization success. The relative importance of each episode of selection is variable among species, and comparative evidence suggests that traits targeted by precopulatory selection often covary in expression with those targeted by postcopulatory selection when assessed across species, although the strength and direction of this association varies considerably among taxa. We tested for correlated evolution between targets of pre- and postcopulatory selection using data on sexual size dimorphism (SSD) and testis size from 151 species of squamate reptiles (120 lizards, 31 snakes). In squamates, male–male competition for mating opportunities often favors large body size, such that the degree of male-biased SSD is associated with the intensity of precopulatory selection. Likewise, competition for fertilization often favors increased sperm production, such that testis size (relative to body size) is associated with the intensity of postcopulatory selection. Using both conventional and phylogenetically based analyses, we show that testis size consistently decreases as the degree of male-biased SSD increases across lizards and snakes. This evolutionary pattern suggests that strong precopulatory selection may often constrain the opportunity for postcopulatory selection and that the relative importance of each selective episode may determine the optimal resolution of energy allocation trade-offs between traits subject to each form of sexual selection.
... Males often possess horns, a precopulatory sexual trait, on the head and/or thorax, which are used in defending breeding tunnels occupied by females (Garcia-Gonzalez & Simmons, 2011;Kijimoto et al., 2009;Simmons & García-González, 2008). Some species exhibit tradeoffs between male horn length and investment in postcopulatory traits such as testes and sperm (Moczek & Nijhout, 2004;Reynolds & Byrne, 2013). Studies in Onthophagus have shown alternative mating strategies where smaller males prioritize investing more in testes size and sperm production over horn investment (Simmons & Emlen, 2006;Simmons & García-González, 2008;Simmons et al., 2007). ...
... Due to limited resources for growth and development, there may potentially be trade-offs in the investment of precopulatory and postcopulatory traits (Moczek & Nijhout, 2004). As there was a high relative investment in horn length, a precopulatory trait, we hypothesized that there would be a low relative investment in postcopulatory traits such as testes weight and sperm length. ...
Sexual size dimorphism (SSD) arises when natural selection and sexual selection act differently on males and females. Male-biased SSD is rarer in insects and usually indicates strong sexual selection pressure on male body size in a species. Patterns of SSD can also vary between populations of species that are exposed to different environmental conditions, such as differing resource availability and diversity. Here, we investigate intraspecific variation in SSD as well as relative investment in precopulatory (horn length) and postcopulatory traits (sperm length and testes weight) in a tropical rainforest dung beetle Onthophagus babirussa across Singapore and Peninsular Malaysia. Overall, three out of four populations displayed significant male-biased SSD, and SSD was greater in populations with smaller overall body size. Average male body size was similar across all populations while female body size was significantly smaller in Singapore, suggesting that the pronounced SSD may also be due to stronger sexual selection on male body size in Singapore populations. All populations showed significant investment in horns as a weapon likely used in male-male competition, while postcopulatory traits showed no clear scaling relationship with body size, suggesting a higher priority on precopulatory sexual traits in the mating system of this species.
... Weapons can also impose energetic costs that reduce viability and fitness [9]. Most studies of energetic costs focus on signalling and growth, which can be ephemeral if weapon growth is episodic [10]. However, they overlook an energetic sink that is omnipresent and interminable-energetic maintenance costs. ...
... Energetic maintenance costs are constant energy sinks that arise from the body's homeostatic biochemical reactions [11]. They represent the 'cost of living while doing nothing' [11] and are distinct from more ephemeral energetic costs of growth [10] and signalling [12]. For sexually selected traits, maintenance costs are massive. ...
The cost-minimization hypothesis proposes that positive allometry in sexually selected traits can be explained if the proportional energetic maintenance costs of weapons decrease as traits increase in size. Energetic maintenance costs are the costs of maintaining homeostasis. They are slow, persistent energy sinks that are distinct from ephemeral costs of growth. Because some tissues expend more energy on maintenance than others, energetic maintenance costs can be inferred from proportional tissue composition. For example, soft tissues require more energy for maintenance than exoskeleton, so an arthropod claw that is 50% soft tissue and 50% exoskeleton would have higher energetic maintenance costs than one that is 30% soft tissue and 70% exoskeleton. I tested the cost-minimization hypothesis using proportional tissue composition as a proxy for energetic maintenance costs in snapping shrimp ( Alpheus heterochaelis and Alpheus estuariensis ) and fiddler crabs ( Uca pugilator ). As predicted, larger weapons comprised proportionally less soft tissue mass and more exoskeleton mass than smaller weapons. Furthermore, I extended cost-minimization to explain trait exaggeration: individuals might exaggerate traits by investing more mass in exoskeleton. As predicted, exoskeleton mass proportional to weapon mass increased as exaggeration increased. These results support and extend the cost-minimization hypothesis to explain positive allometry and weapon exaggeration.
... In addition, we investigated male investment in a precopulatory trait (horn length) and postcopulatory traits (testes weight and sperm length) by calculating static allometry, a widely used 2 tool in quantifying relative investment in traits as a function of body size (Eberhard et al. , 2018). Prior studies suggest that there may be potential trade-offs in the investment of precopulatory and postcopulatory traits given the limited resources for development (Moczek & Nijhout, 2004). As beetle horns are important in mate acquisition (Simmons & Ridsdill-Smith, 2011), we tested the hypothesis that there would be a high investment in beetle horns, hence a positive allometry and that the allometric coefficient for postcopulatory traits would be lower than that of horns. ...
... Due to limited resources for growth and development, there may potentially be trade-offs in the investment of precopulatory and postcopulatory traits (Moczek & Nijhout, 2004). As there was a high relative investment in horn length, a precopulatory trait, we hypothesized that there would be a low relative investment in postcopulatory traits such as testes weight and sperm length. ...
Sexual size dimorphism (SSD) arises when natural selection and sexual selection act differently on males and females. Rensch’s rule predicts that SSD increases with body size in species when males are the larger sex. However, male-biased SSD is rare in insects and the rule does not always hold between species and even among populations. Here, we investigate intra-specific variation in SSD as well as relative investment in precopulatory (horn length) and postcopulatory traits (sperm length and testes weight), in a tropical rainforest dung beetle Onthophagus babirussa across Singapore and Peninsular Malaysia. Overall, three out of four populations displayed significant male-biased SSD but contrary to Rensch’s rule, SSD was greater in populations with smaller overall body size. Average male body size was similar across all populations, but female body size differed significantly suggesting that the pronounced SSD may also be due to weaker fecundity selection on female body size. Across all populations, horn length showed a strong positive static allometry while postcopulatory traits showed negative allometry (in all but one population), which suggests an evolutionary trade-off between precopulatory and postcopulatory traits in this species.
... Because most resource allocation to traits making up the adult body (e.g., Oberlander 1985;Nijhout and Emlen 1998;Moczek and Nijhout 2004;Rolff et al. 2019;Mirth et al. 2021) and immunity (e.g., Barnes and Siva-Jothy 2000;Cotter et al. 2004;Triggs and Knell 2012) takes place during larval or nymphal stages in insects, these juveniles can adjust their resource allocation to traits of different functions in response to socio-sexual cues, leading to potential trade-offs between different body traits (Nijhout and Emlen 1998;Simmons and Emlen 2006;Luecke and Kopp 2019). To date, only a few studies have investigated how male insects fine-tune their investment in reproduction during growth and development as a response to potential sperm competition risk. ...
... Therefore, males may be able to donate varying portions of testis volumes to spermatogenesis and other functions in response to sperm competition environment (Lü pold et al. 2020). Because a resource used for 1 trait may not be used for another, potential tradeoffs between traits of different functions may occur (Nijhout and Emlen 1998;Moczek and Nijhout 2004;Luecke and Kopp 2019). Based on the results from the present study and current knowledge about testicular components and functions, we suggest that in response to the presence of conspecific social cues E. kuehniella male larvae may increase investment in fertile sperm cells and reduce investment in other tissues of the testes. ...
Socio-sexual environment can have critical impacts on reproduction and survival of animals. Consequently, they need to prepare themselves by allocating more resources to competitive traits that give them advantages in the particular social setting they have been perceiving. Evidence shows that a male usually raises his investment in sperm after he detects the current or future increase of sperm competition because relative sperm numbers can determine his paternity share. This leads to the wide use of testis size as an index of the sperm competition level, yet testis size does not always reflect sperm production. To date, it is not clear whether male animals fine-tune their resource allocation to sperm production and other traits as a response to social cues during their growth and development. Using a polygamous insect Ephestia kuehniella, we tested whether and how larval social environment affected sperm production, testis size and body weight. We exposed the male larvae to different juvenile socio-sexual cues and measured these traits. We demonstrate that regardless of sex ratio, group-reared males produced more eupyrenes (fertile and nucleate sperm) but smaller testes than singly-reared ones, and that body weight and apyrene (infertile and anucleate sperm) numbers remained the same across treatments. We conclude that the presence of larval social, but not sexual cues, is responsible for the increase of eupyrene production and decrease of testis size. We suggest that male larvae increase investment in fertile sperm cells and reduce investment in other testicular tissues in the presence of conspecific juvenile cues.
... This suggests that the autotomy of its weapons freed up resources that could be invested elsewhere (Joseph et al., 2017). Similarly, the ablation of genital precursor cells in juvenile male horned scarab beetles Onthophagus taurus (Schreber, 1759) results in the growth of larger horns compared to unablated males (Moczek & Nijhout, 2004). Such studies indicate that the investment costs of pre-and post-copulatory attributes reciprocally limit their expression. ...
... Such studies indicate that the investment costs of pre-and post-copulatory attributes reciprocally limit their expression. In the leaffooted cactus bug and the horned scarab beetle, the trade-off between investing in pre-and post-copulatory attributes occurs prior to maturation (Moczek & Nijhout, 2004;Joseph et al., 2017). The question that we ask here is as follows: Do costs associated with having precopulatory attributes affect post-copulatory energy budgets and reproductive investment post maturation, that is during the adult stage? ...
Morphological structures used as weapons in male‐male competition are not only costly to develop but are also probably costly to maintain during adulthood. Therefore, having weapons could reduce the energy available for other fitness‐enhancing actions, such as postcopulatory investment. We tested the hypothesis that armed males make lower postcopulatory investments than unarmed males, and that this difference will be most pronounced under food‐limited conditions. We performed two experiments using the male‐dimorphic bulb mite Rhizoglyphus robini, in which males are either armed ‘fighters’ or unarmed ‘scramblers’. Firstly, we tested whether fighters and scramblers differed in their reproductive output after being starved or fed for one or two weeks. Secondly, we measured the reproductive output of scramblers and fighters (starved or fed) after one, two or three consecutive matings. Scramblers sired more offspring than fighters after one week, but scramblers and fighters only sired a few offspring after two weeks. Scramblers also sired more offspring than fighters at the first mating, males rarely sired offspring after consecutive matings. Contrary to our hypothesis, the fecundity of starved and fed males did not differ. The higher reproductive output of scramblers suggests that, regardless of nutritional state, scramblers make larger postcopulatory investments than fighters. Alternatively, (cryptic) female choice generally favours scramblers. Why the morphs differed in their reproductive output is unclear. Neither morph performed well relatively late in life or after multiple matings. It remains to be investigated to what extent the apparent scrambler advantage contributes to the maintenance and evolution of male morph expression.
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... Dung beetles have been shown to display high phenotypic plasticity in certain traits in response to resource availability (Moczek & Nijhout, 2004) and environmental change (Alves & Hernández, 2017;Emlen, 1994;Moczek, 2002;Pomfret & Knell, 2006). In particular, the morphology of males of the same species has been found to vary greatly as a result of resource quality (Moczek & Emlen, 2000;Moczek & Nijhout, 2004), and differences in horn size and shape, both within and between species, are well documented (e.g., Emlen, Marangelo, Ball, & Cunningham, 2005). ...
... Dung beetles have been shown to display high phenotypic plasticity in certain traits in response to resource availability (Moczek & Nijhout, 2004) and environmental change (Alves & Hernández, 2017;Emlen, 1994;Moczek, 2002;Pomfret & Knell, 2006). In particular, the morphology of males of the same species has been found to vary greatly as a result of resource quality (Moczek & Emlen, 2000;Moczek & Nijhout, 2004), and differences in horn size and shape, both within and between species, are well documented (e.g., Emlen, Marangelo, Ball, & Cunningham, 2005). Intraspecific differences in morphological traits are therefore likely to be easily detected where they occur, making dung beetles the ideal study group to assess whether land use change and associated changes in resource availability may be causing intraspecific differences in functional traits. ...
Functional traits and functional diversity measures are increasingly being used to examine land use effects on biodiversity and community assembly rules. Morphological traits are often used directly as functional traits. However, behavioral characteristics are more difficult to measure. Establishing methods to derive behavioral traits from morphological measurements is necessary to facilitate their inclusion in functional diversity analyses. We collected morphometric data from over 1,700 individuals of 12 species of dung beetle to establish whether morphological measurements can be used as predictors of behavioral traits. We also compared morphology among individuals collected from different land uses (primary forest, logged forest, and oil palm plantation) to identify whether intraspecific differences in morphology vary among land use types. We show that leg and eye measurements can be used to predict dung beetle nesting behavior and period of activity and we used this information to confirm the previously unresolved nesting behavior for Synapsis ritsemae. We found intraspecific differences in morphological traits across different land use types. Phenotypic plasticity was found for traits associated with dispersal (wing aspect ratio and wing loading) and reproductive capacity (abdomen size). The ability to predict behavioral functional traits from morphology is useful where the behavior of individuals cannot be directly observed, especially in tropical environments where the ecology of many species is poorly understood. In addition, we provide evidence that land use change can cause phenotypic plasticity in tropical dung beetle species. Our results reinforce recent calls for intraspecific variation in traits to receive more attention within community ecology.
... Although organisms must use a finite energy budget to accumulate body mass, the ubiquity of modularity in organismal systems ranging from mammals to fishes (Esteve-Altava, 2017; Larouche, Cloutier, & Zelditch, 2015) without obvious trade-offs between adjacent tissues (reviewed in Warren & Iglesias, 2012) suggests that simple economic predictions between morphological modules may not have much explanatory power for understanding the evolution of most ontogenetic pathways without a more detailed perspective of lineage-specific energy budgets and life history. While investment trade-offs between morphological modules have provided evidence for the expectations of the ETH in a few animal lineages (Emlen, 2001;Liao et al., 2016;Moczek & Nijhout, 2004), the large number of studies that have failed to recover support in other lineages suggests that the broad expectations of the ETH are far from a universal rule (reviewed in Warren & Iglesias, 2012). ...
... While increases in the energetic cost of one morphological module do not often lead to negatively correlated changes in another, this does not preclude the possibility that some modules are in fact faced with a possible deficit in energy as sexual selection emphasizes trait investment (Moczek & Nijhout, 2004). However, without a detailed understanding of the ecology and energy requirements of a species, it is not clear to what extent organisms can offset deficits through changes in behavior or feeding ecology. ...
Trade-offs associated with sexual size dimorphism (SSD) are well documented across the Tree of Life. However, studies of SSD often do not consider potential investment trade-offs between metabolically expensive structures under sexual selection and other morphological modules. Based on the expectations of the expensive tissue hypothesis, investment in one metabolically expensive structure should come at the direct cost of investment in another. Here, we examine allometric trends in the ontogeny of oyster toadfish (Opsanus tau) to test whether investment in structures known to have been influenced by strong sexual selection conform to these expectations. Despite recovering clear changes in the ontogeny of a sexually selected trait between males and females, we find no evidence for predicted ontogenetic trade-offs with metabolically expensive organs. Our results are part of a growing body of work demonstrating that increased investment in one structure does not necessarily drive a wholesale loss of mass in one or more organs.
... To reveal resource allocation trade-offs, it is necessary to perform experimental studies where one of the traits in question can be manipulated in isolation, to reveal effects on other traits (Roff, 2002). To date, exceptionally few studies have used experimental manipulations to examine the relationship between pre-and postcopulatory traits; those that have employed an experimental approach have reported evidence of resource allocation trade-offs between sexually selected pre-and post-copulatory traits (Moczek & Nijhout, 2004;Fry, 2006;Simmons & Emlen, 2006;Joseph et al., 2017). The scarcity of studies is likely a result of the difficulty in manipulating allocation to isolated traits, yet these experimental manipulations remain a powerful tool for uncovering allocation trade-offs among life-history traits (Simmons et al., 2017). ...
... To date, few studies have experimentally investigated resource allocation trade-offs among pre-and post-copulatory traits (Simmons et al., 2017). In one well-studied case, onthophagine dung beetles, males experimentally prevented from growing horns had increased relative investment in testicular tissue (Simmons & Emlen, 2006), whereas males prevented from developing primary genitalia increased their allocation to horn growth (Moczek & Nijhout, 2004). In our study, the behavioural feature of weapon autotomy provided an opportunity to prevent weapon development with minimal potential injury and detrimental effects to developing insects and resulted in increased allocation of resources to testes growth. ...
Theory predicts a trade-off between sexually selected weapons used to secure mates and post-copulatory traits used to maximize fertilization success. However, individuals that have a greater capacity to acquire resources from the environment may invest more in both pre- and post-copulatory traits, and trade-offs may not be readily apparent. Here, we manipulate the phenotype of developing individuals to examine allocation trade-offs between weapons and testes in Mictis profana (Hemiptera: Coreidae), a species where the hind legs are sexually selected weapons used in contests over access to females. We experimentally prevented males from developing weapons by inducing them to autotomize their hind legs before the final moult to adulthood. We compared trait expression in this group to males where autotomy was induced in the mid-legs, which are presumably not under sexual selection to the same extent. We found males without weapons invested proportionally more in testes mass than those with their mid-legs removed. Males that developed to adulthood without weapons did not differ from the mid-leg removal group in other traits potentially under precopulatory sexual selection, other post-copulatory traits or naturally selected traits. In addition, a sample of adult males from the same population in the wild revealed a positive correlation between investment in testes and weapons. Our study presents a critical contribution to a growing body of literature suggesting the allocation of resources to pre- and post-copulatory sexual traits is influenced by a resource allocation trade-off and that this trade-off may only be revealed with experimental manipulation.
... In accordance with a trade-off (Zera & Harshman, 2001), multiple studies have found negative phenotypic correlations between investment in pre-and postcopulatory traits at different hierarchical levels: Across species of the same taxa (evolutionary trade-offs; Dines et al., 2015;Dunn et al., 2015;Simmons & Emlen, 2006), within populations (populationlevel trade-offs; Eberhard, 2009a,b;Hayward & Gillooly, 2011) and even within individuals of the same population (allocation trade-offs; Moczek & Nijhout, 2004;Simmons & Emlen, 2006;Somjee et al., 2017). Yet, other studies have found positive or no correlations in competitive investment before and after mating across species, within populations or within individuals (Dziminski et al., 2010;Ferrandiz-Rovira et al., 2014;Lüpold et al., 2015;Painting & Holwell, 2013;Parker et al., 2013;Supriya et al., 2018Supriya et al., , 2019. ...
Sexually selected weapons used to monopolize mating opportunities are predicted to trade-off with traits used in competition for fertilization. Yet, the limited size range typically found among adults of a species often precludes clear comparisons between population-level and individual-level relative trait investment. The jousting weevil, Brentus anchorago (Coleoptera: Brentidae), varies more than 26-fold in body mass, which is among the most extreme adult body size ranges of any solitary terrestrial species. We reveal a trade-off at a population level: hypermetric scaling in male weapons (slope = 1.59) and a closely mirrored reversal in allocation to postcopulatory traits (slope = 0.54). Yet, at the individual level, we find the opposite pattern; males that invest relatively more in weapons for their size class also invest more in postcopulatory traits. Across 36 dung beetle and 41 brentine weevil species, we find the allometric slope explains more trait variation at larger body size ranges; in brentines, population-level scaling patterns become more detectable in species with a larger range in adult body size. Our findings reveal that population-level allometries and individual-level trade-offs can both be important in shaping relative trait allocation; we highlight that the adult body size range is rarely examined but may be integral to gaining a deeper understanding of trade-offs in reproductive allocation.
... Theory predicts that post-copulatory processes can oppose pre-copulatory selection on a given trait if investment in corresponding fitness components is drawn from the same limited resources, or if the genetic covariance among fitness components is negative (Roff and Fairbairn 2007;Parker et al. 2013). Accordingly, inter-and intraspecific comparisons across several lineages, including reptiles, have shown that traits typically subjected to pre-copulatory selection trade off with those under postcopulatory selection (Moczek and Nijhout 2004;Fitzpatrick et al. 2012;Dines et al. 2015;Kahrl et al. 2016;Somjee et al. 2018). On the other hand, when there is high variance in resource acquisition, as can occur in the wild, individuals with high acquisition are predicted to invest in and achieve high fitness through both pre-and Table 1 Summary of coefficient estimates a,b from linear regressions with corresponding error distributions, carried out separately for each measure of fitness as the response variable when pooling data from May and July: reproductive success (total number of offspring), mating success (total number of mates), average mate fecundity (mean fecundity across all mates), and competitive fertilization success (mean proportion of offspring sired across all mates, adjusted for the number of competing males), with size quartile (ordinal), month (categorical) and their interaction included as predictors. ...
In promiscuous species, fitness estimates obtained from genetic parentage may often reflect both pre- and post-copulatory components of sexual selection. Directly observing copulations can help isolate the role of pre-copulatory selection, but such behavioral data are difficult to obtain in the wild and may also overlook post-copulatory factors that alter the relationship between mating success and reproductive success. To overcome these limitations, we combined genetic parentage analysis with behavioral estimates of size-specific mating in a wild population of brown anole lizards (Anolis sagrei). Males of this species are twice as large as females and multiple mating among females is common, suggesting the scope for both pre- and post-copulatory processes to shape sexual selection on male body size. Our genetic estimates of reproductive success revealed strong positive directional selection for male size, which was also strongly associated with the number of mates inferred from parentage. In contrast, a male’s size was not associated with the fecundity of his mates or his competitive fertilization success. By simultaneously tracking copulations in the wild via the transfer of colored powder to females by males from different size quartiles, we independently confirmed that large males were more likely to mate than small males. We conclude that body size is primarily under pre-copulatory sexual selection in brown anoles, and that post-copulatory processes do not substantially alter the strength of this selection. Our study also illustrates the utility of combining both behavioral and genetic methods to estimate mating success to disentangle pre- and post-copulatory processes in promiscuous species.
... It is possible that this reduced elongation rate may be due to the increase in the degree of growth occurring along the dorso-ventral axis in this species, perhaps due to a developmental trade-off between the two axes of growth. In developing organisms, growth is limited by the amount of circulating resources, such as amino acids and insulins, for which different organs, tissues, and even cells can compete (Gawne et al., 2020;Klingenberg & Frederik Nijhout, 1998;Moczek & Nijhout, 2004;Nijhout & Emlen, 1998). If we consider anterior-posterior elongation and dorso-ventral growth two separate traits with cells needing to divide in "competing" directions, we posit that developing both an exaggerated anterior process and a medial dorso-ventral expansion is less likely to occur (Nijhout & Emlen, 1998). ...
Membracids (family: Membracidae), commonly known as treehoppers, are recognizable by their enlarged and often elaborated pronota. Much of the research investigating the development and evolution of this structure has focused on the fifth instar to adult transition, in which the pronotum undergoes the largest transformation as it takes on adult identity. However, little is known about the earlier nymphal stages, the degree to which the pronotum develops at these timepoints, and how development has changed relative to the ancestral state. Here, we studied the nymphal stages and adults of five morphologically distinct membracid species and of Aetalion reticulatum (family: Aetalionidae), the outgroup which was used as an ancestral state proxy. We found that shape differentiation in the pronotum of membracids can start as early as the second instar stage. Most shape differentiation occurs within the nymphal stages and not in the embryo since the shape of the first-instar pronotum did not differ from the outgroup species in all but one species we investigated. We found the anterior-posterior axis of the pronotum elongated at a faster relative rate in membracid species than in A. reticulatum, which contributed to the development of exaggerated pronotal size. Finally, we found differences in the morphogenesis of shape across species. We suggest this is due to the developmental and evolutionary divergence of differential growth patterning of the dorsal surface of the pronotum, not only across species, but also between stages within the same species. This lability may contribute to the evolvability and diversification of the membracid pronotum.
... Individuals appear to be able to redirect resources to testes growth when experimentally prevented from investing in a precopulatory weapon, but this phenotypic plasticity diminishes upon adulthood. Although the proximate drivers and timing of such trade-offs have previously been focused on in holometabolous insects, given their fixed resource budget and rapid development phase as pupae (Emlen, 2001;Moczek & Nijhout, 2004;Nijhout & Emlen, 1998;Tomkins et al., 2005), clearly similar patterns exist in hemimetabolous insects and potentially other animals that feed continuously throughout development. Sexually selected traits represent a fertile testing ground for further empirical exploration of the ontogeny of life history trade-offs (Lande, 2019;McDermott & Safran, 2021;Riska, 1986). ...
A longstanding goal of evolutionary biology is to understand among-individual variation in resource allocation decisions and the timing of these decisions. Recent studies have shown that investment in elaborate and costly weapons can result in trade-offs with investment in testes. In this study, we ask at what point plasticity in resource allocation to these different structures ceases during development, if at all? Furthermore, can individuals tailor their reproductive behavior to accompany structural changes? We experimentally addressed these questions in the insect Narnia femorata, quantifying resource reallocation across development for the first time, using a phenotypic engineering approach. To investigate whether allocation plasticity diminishes throughout ontogeny, we induced weapon loss at a range of different developmental stages and examined subsequent testes mass and reproductive behavior. We found that relative testes mass increased as weapon investment decreased, implying a direct trade-off between testes and weapon investment. However, autotomy post-adulthood ceased to induce larger testes mass. Intriguingly, losing a weapon while young was associated with extended adult mating duration, potentially enabling compensation for reduced fighting ability. Our results highlight the importance of examining the ontogeny of trade-offs between reproductive traits and the flexibility of the relationship between reproductive morphology and behavior.
... Furthermore, there may be compensation between male elongated chelicerae and neighboring structures (Tomkins et al. 2005). Although a few studies have revealed trade-offs between weapons and neighboring structures in some beetles (Nijhout and Emlen 1998;Emlen 2001;Moczek and Nijhout 2004;Simmons and Emlen 2006), more studies provide support for compensation (see references above). In addition, resource allocation trade-offs seem to be especially unlikely to occur in spiders because spiders do not develop closed developmental systems (i.e., holometabolous) (Foelix 2011). ...
A core assumption of sexual selection theory is that sexually selected weapons, specialized morphological structures used directly in male contests, can improve an individual’s reproductive success but only if the bearer can overcome associated costs, the negative effects on the bearer’s fitness components. However, recent studies have shown that producing and wielding exaggerated weapons may not necessarily be costly. Rather, some traits can be selected for supporting, or compensating for, the expense of producing and wielding such exaggerated weapons. In the ant-mimicking jumping spider Myrmarachne gisti, exaggerated chelicerae are borne only by adult males and not females, showing sexual dimorphism and steep positive allometry with body size. Here, we determine the potential benefits of bearing exaggerated chelicerae during male contests and explore the potential for costs in terms of prey -capture efficiency and compensation between chelicera size and neighbouring trait size. While males with longer chelicerae won most of their malemale contests, we found no significant differences in prey -capture efficiency between males and females regardless of whether prey were winged or flightless. Males’ elongated chelicerae thus do not impede their efficiency at capturing prey. Furthermore, we found that the sizes of all neighbouring traits are positively correlated with chelicera size, suggesting that these traits may be under correlational selection . Taken together, our findings suggest that M. gisti males armed with the exaggerated chelicerae that function as weapons win more fights at limited cost for performance in prey -capture and compensate for neighbouring structures.
... The representation of dung beetle traits (e.g., body size, nesting strategy, dispersal ability, activity period and diet preference) within and amongst dung beetle species changes with resource availability (Moczek and Nijhout 2004) and environmental factors (Alves and Hernández 2017;Barragán et al. 2011;Nichols et al. 2013;Da Silva and Hernández 2014). Habitat structure (vegetation and litter cover), which varies with management strategy, can exclude certain groups (e.g., Steenkamp and Chown 1996;Tixier et al. 2015). ...
Insects perform many ecosystem functions, yet their responses to disturbance can be unpredictable. Changes in climate may interact with land use disturbances, and given that arthro-pod species diversity, abundance, and traits within assemblages vary with habitat structure and climatic variables, ecological function may be impaired. Here, we assessed how dung beetle species richness, abundance, functional diversity, mean body size and body size inequality (which can signal assemblage stress responses) varied with climatic, management and habitat variables on livestock farms and protected areas across a rainfall gradient (138-381 mm/year) in arid/semi-arid shrubland (Karoo, South Africa, an area for which entomological biodiversity is relatively poorly known), during a prolonged drought. Species richness was similar between farms and protected areas, but abundance was greater in protected areas. Farms tend to be dominated by sheep in this region, and the type of dung and paucity of dung diversity, along with use of anthelmintics may explain this reduced abundance. Species richness and abundance increased with mammalian herbivore stocking rates and rainfall. Most recent rainfall best predicted species richness, but abundance was best explained by the long-term measure of rainfall (Mean Annual Precipitation). Functional diversity showed no patterns with the environmental or management variables we measured. Mean body length and size variation did not differ between protected areas and farms, but the spread of beetle sizes was more even as vegetation cover increased and soil clay content decreased. Future climate projections indicate extreme declines in rainfall in this area, and our results suggest that this would dramatically impact dung beetle communities. Maintaining vegetation cover may help mitigate effects of climate change.
... One of the most commonly invoked mechanisms for trade-offs is that they arise when different traits or functions compete for the same pool of finite resources such energy, time, or space (Zera and Harshman 2001;Garland et al. 2022). Such allocation trade-offs play a central role in explaining diverse aspects of organismal biology, ranging from the evolution of different life history strategies (Van Noordwijk and de Jong 1986;Roff 1992) to developmental constraints on the size of differ-ent morphological structures (Nijhout and Emlen 1998;Moczek and Nijhout 2004). Similar allocation tradeoffs have also been proposed to mediate biotic interactions with predators and herbivores (e.g., Coley et al. 1985), competitors (Grime 1977), and context dependent changes along elevational and latitudinal gradients (Hargreaves et al. 2014;Louthan et al. 2015;Paquette and Hargreaves 2021). ...
Synopsis
It has long been known that the outcome of species interactions depends on the environmental context in which they occur. Climate change research has sparked a renewed interest in context-dependent species interactions because rapidly changing abiotic environments will cause species interactions to occur in novel contexts and researchers must incorporate this in their predictions of species’ responses to climate change. Here, we argue that predicting how the environment will alter the outcome of species interactions requires an integrative biology approach that focuses on the traits, mechanisms, and processes that bridge disciplines such as physiology, biomechanics, ecology, and evolutionary biology. Specifically, we advocate for quantifying how species differ in their tolerance and performance to both environmental challenges independent of species interactions, and in interactions with other species as a function of the environment. Such an approach increases our understanding of the mechanisms underlying outcomes of species interactions across different environmental contexts. This understanding will help determine how the outcome of species interactions affects the relative abundance and distribution of the interacting species in nature. A general theme that emerges from this perspective is that species are unable to maintain high levels of performance across different environmental contexts because of trade-offs between physiological tolerance to environmental challenges and performance in species interactions. Thus, an integrative biology paradigm that focuses on the trade-offs across environments, the physiological mechanisms involved, and how the ecological context impacts the outcome of species interactions provides a stronger framework to understand why species interactions are context dependent.
... Studies of potential sperm competition in genus Onthophagus provided insights into evolutionary and ecological significance of testis-horn size relationships [31,32]. Moreover, a trade-off between male genitalia development and horn size determination has been reported using O. taurus [33]. Thus, we sought candidate metabolites that are specifically detected by the male-female comparison or the large-small male comparison (see above). ...
Organisms alter their phenotypes in response to changing environmental conditions. The developmental basis of this phenomenon, phenotypic plasticity, is a topic of broad interest in many fields of biology. While insects provide a suitable model for studying the genetic basis of phenotypic plasticity, the physiological aspects of plasticity are not fully understood. Here, we report the physiological basis of polyphenism, an extreme form of phenotypic plasticity by utilizing a dung beetle species, Onthophagus taurus. We highlighted the metabolome between sexes as well as two distinct male morphs—large and small horns. Unlike results from previous transcriptomic studies, the comparative metabolomic study revealed that differences in metabolite level were more prominent between animals with different body sizes than different sexes. Our results also indicate that specific metabolites and biochemical pathways may be active during horn size determination.
... Dung beetles (Coleoptera: Scarabaeinae) have been widely studied from a functional perspective, because of their important ecological roles in nutrient cycling, secondary seed dispersal, and parasite control (Nichols et al., 2008;Slade et al., 2016). Also, dung beetles are a good model in functional diversity studies because of their high phenotypic plasticity in response to resources availability and environmental conditions (Moczek & Nijhout, 2004). However, previous functional studies with these insects exhibit several limitations. ...
1. Functional diversity has been defined as the value, range, distribution, and relative
abundance of the functional traits of individuals that belong to an ecosystem. Thus,
the functional response of organisms to environmental disturbances depends
largely on their functional traits.
2. Here, we evaluated dung beetle functional diversity associated to the Atlantic
Forest replacement using a matrix with 25 functional traits (10 morphological, four
ethological, and 11 physiological). We compared functional diversity among native
and disturbed habitats with a multi and single trait approach.
3. Contrary to previous studies, habitats with higher disturbance (open pasture) exhibited
higher functional diversity compared to native forests, which could be explained by the
incorporation of physiological response traits. Species of open disturbed habitats
showed extreme values of such traits, explaining the observed pattern.
4. The inclusion of several traits that represent both species ecology and morphology,
and their physiology, generates different results to those observed in previous
functional studies. This highlights the importance of including a large variety of
functional traits in future functional diversity studies.
5. We propose that functional traits must (1) be carefully chosen according to their biological
and functional basis; (2) represent species ecology and physiology; and (3) include both
effect and response traits. In addition, we consider it is extremely relevant to include a
multi and single trait approach in functional diversity studies. A combination of all these
considerations will provide a more realistic and complete overview of functional diversity
patterns and the potential consequences of human disturbance on ecosystem functioning.
... Dung beetles (Coleoptera: Scarabaeinae) have been widely studied from a functional perspective, because of their important ecological roles in nutrient cycling, secondary seed dispersal, and parasite control (Nichols et al., 2008;Slade et al., 2016). Also, dung beetles are a good model in functional diversity studies because of their high phenotypic plasticity in response to resources availability and environmental conditions (Moczek & Nijhout, 2004). However, previous functional studies with these insects exhibit several limitations. ...
Functional diversity has been defined as the value, range, distribution, and relative abundance of the functional traits of individuals that belong to an ecosystem. Thus, the functional response of organisms to environmental disturbances depends largely on their functional traits.
Here, we evaluated dung beetle functional diversity associated to the Atlantic Forest replacement using a matrix with 25 functional traits (10 morphological, four ethological, and 11 physiological). We compared functional diversity among native and disturbed habitats with a multi and single trait approach.
Contrary to previous studies, habitats with higher disturbance (open pasture) exhibited higher functional diversity compared to native forests, which could be explained by the incorporation of physiological response traits. Species of open disturbed habitats showed extreme values of such traits, explaining the observed pattern.
The inclusion of several traits that represent both species ecology and morphology, and their physiology, generates different results to those observed in previous functional studies. This highlights the importance of including a large variety of functional traits in future functional diversity studies.
We propose that functional traits must (1) be carefully chosen according to their biological and functional basis; (2) represent species ecology and physiology; and (3) include both effect and response traits. In addition, we consider it is extremely relevant to include a multi and single trait approach in functional diversity studies. A combination of all these considerations will provide a more realistic and complete overview of functional diversity patterns and the potential consequences of human disturbance on ecosystem functioning.
... Rapidly growing organs may be most sensitive to allocation tradeoffs. [102][103][104] Resource limitation during rapid growth has been suggested to shape the relative allocation to sexually selected traits. For example this is the potential cause of the curved allometries in lucanid beetles [105] and other holometabolous insects where growth occurs relatively quickly during a non-feeding stage. ...
Sexual selection drives the evolution of some of the most exaggerated traits in nature. Studies on sexual selection often focus on the size of these traits relative to body size, but few focus on energetic maintenance costs of the tissues that compose them, and the ways in which these costs vary with body size. The relationships between energy use and body size have consequences that may allow large individuals to invest disproportionally more in sexually selected structures, or lead to the reduced per‐gram maintenance cost of enlarged structures. Although sexually selected traits can incur energetic maintenance costs, these costs are not universally high; they are dependent on the relative mass and metabolic activity of tissues associated with them. Energetic costs of maintenance may play a pervasive yet little‐explored role in shaping the relative scaling of sexually selected traits across diverse taxa. Large animals generally have lower relative rates of energy use compared to small ones. In many diverse groups, large animals also invest in disproportionately larger sexually selected traits. The economy of energy gained by large size may play an important role in shaping the positive scaling of sexually selected traits.
... Constraints on the growth of elaborate sexual traits could be a consequence of limited resource availability (Knell et al. 2004;Tomkins et al. 2005). In holometabolous insects, competition for resources can occur among growing body parts within the pupa (Nijhout & Wheeler 1996;Moczek & Nijhout 2004). The development of a disproportionally large sexual trait is expected to constrain growth. ...
Differentiation in sexual traits among populations is one of the major predictions of theories of sexual selection and sexual conflict. A balance between maximizing reproductive benefits and minimizing survival costs could explain variation in sexual traits within and between populations. The false blister beetle Oedemera sexualis (Coleoptera: Oedemeridae) has exaggerated sexual traits, that is, sexually dimorphic hindlegs. In this study, we characterized scaling relationships in populations of O. sexualis to evaluate the determinants of sexual trait variation in the species. We quantified sexual dimorphism in body size and hindleg sizes in three representative populations based on distance measurements and an elliptical Fourier analysis. We found significant variation in the degree of sexual dimorphism for body and hindleg sizes among populations. In particular, differentiation in the male hind femur shape, especially the femur width, was conspicuous. Scaling relationships between male hind femur width and body size were best described by logistic models, showing that increases in male hind femur width were constrained for large individuals in all three populations. The degree of constrained growth of the hind femur width differed among populations in accordance with the population means, while the basal growth rates did not. Populations with smaller mean values for sexual traits showed more limited sexual trait exaggeration, contrary to the predictions based on resource competition among body parts. The latitudinal cline in femur widths suggests that environmental constraints on exaggeration might be responsible for sexual trait diversification in O. sexualis.
... Phenotypic engineering is a powerful experimental technique for investigating trait allocation patterns and trade-offs (Zera & Harshman, 2001). Researchers can, for example, prevent or reduce investment in one trait and then examine the resulting change in the expression of other traits (Moczek & Nijhout, 2004;Sekii et al., 2013). Growth in certain traits after the procedure provides evidence for a resource allocation trade-off occurs between the manipulated trait and the trait in question (Zera & Harshman, 2001). ...
Social conditions can alter the allocation of resources to reproductive traits. For example, an increase in social density during development is frequently associated with an increase in the testes mass of males. Sperm competition theory assumes that increased investment in testes should come at the expense of investing into precopulatory traits, such as sexually selected weaponry. However, much remains unknown about the role of the social context on the concurrent, relative investment in both testes and weapons. We found that the leaf‐footed cactus bug, Narnia femorata (Hemiptera: Coreidae), grew nearly 20% larger testes when raised in high social densities. In addition to manipulating social density, we used autotomy (limb loss) to limit investment in their hind‐limb weapon during development. At low densities, we found that those that lost a weapon during development grew larger testes by adulthood, supporting previous work demonstrating a weapons‐testes trade‐off. However, at high social densities, males that dropped a hind limb did not grow larger testes, though testes were already large at this density. These results underscore the importance of the social context to resource allocation patterns within the individual.
... 47) and other hydroporines, is not in a different position relative to that of other dytiscid larvae, but appears posteriad due to elongation of the anterior portion of the cephalic capsule into the nasale, another structure adapted for specialized feeding habits (Matta, 1983;Friis et al., 2003;Hayashi & Ohba, 2018). Furthermore, this could also be a result of shortening the posterior region of the cephalic capsule due to a developmental trade-off for lengthening of the nasale, given an increase in certain structures is known to result in compensatory decreases in other anatomical features (Nijhout & Wheeler, 1996;Moczek & Nijhout, 2004), including those located near the exaggerated trait (Emlen, 2001). These aspects render homology assessment of the position of the larval cerebrum both within Dytiscidae, and among dytiscids and hygrobiids problematic. ...
... The development of mandible traits and fighting behaviour requires many resources [4,[23][24][25]. Because tonic immobility does not consume energy compared with moving escape tactics [26], tonic immobility may be the optimal tactic for males with larger mandibles. ...
Tonic immobility and escape are adaptive anti-predator tactics used by many animals. Escape requires movement, whereas tonic immobility does not. If anti-predator tactics relate to weapon size, males with larger weapons may adopt tonic immobility, whereas males with smaller weapons may adopt escape. However, no study has investigated the relationship between weapon size and anti-predator tactics. In this study, we investigated the relationship between male weapon size and tonic immobility in the beetle Gnathocerus cornutus. The results showed that tonic immobility was more frequent in males with larger weapons. Although most studies of tonic immobility in beetles have focused on the duration, rather than the frequency, tonic immobility duration was not affected by weapon size in G. cornutus. Therefore, this study is the first, to our knowledge, to suggest that the male weapon trait affects anti-predator tactics.
... Onthophagus beetles that were experimentally prevented from developing horns developed larger relative testes (Simmons and Emlen 2006). Conversely, experimental ablation of the precursor cells of genitalia in Onthophagus resulted in exaggerated growth of horns (Moczek and Nijhout 2004). In some systems, there is a positive correlation between investment in precopulatory and postcopulatory phenotypes (Kelley et al. 2014), which could occur if overall resource acquisition increases (Devigili et al. 2013). ...
The Caribbean island biota is characterized by high levels of endemism, the result of an interplay between colonization opportunities on islands and effective oceanic barriers among them. A relatively small percentage of the biota is represented by ‘widespread species’, presumably taxa for which oceanic barriers are ineffective. Few studies have explored in detail the genetic structure of widespread Caribbean taxa. The cobweb spider Spintharus flavidus Hentz, 1850 (Theridiidae) is one of two described Spintharus species and is unique in being widely distributed from northern N. America to Brazil and throughout the Caribbean. As a taxonomic hypothesis, Spintharus “flavidus ” predicts maintenance of gene flow among Caribbean islands, a prediction that seems contradicted by known S. flavidus biology, which suggests limited dispersal ability. As part of an extensive survey of Caribbean arachnids (project CarBio), we conducted the first molecular phylogenetic analysis of S. flavidus with the primary goal of testing the ‘widespread species’ hypothesis. Our results, while limited to three molecular loci, reject the hypothesis of a single widespread species. Instead this lineage seems to represent a radiation with at least 16 species in the Caribbean region. Nearly all are short range endemics with several distinct mainland groups and others being single island endemics. While limited taxon sampling, with a single specimen from S. America, constrains what we can infer about the biogeographical history of the lineage, clear patterns still emerge. Consistent with limited overwater dispersal, we find evidence for a single colonization of the Caribbean about 30 million years ago, coinciding with the timing of the GAARLandia landbridge hypothesis. In sum, S. “flavidus” is not a single species capable of frequent overwater dispersal, but rather a 30 my old radiation of single island endemics that provides preliminary support for a complex and contested geological hypothesis.
... In T. angusticollis, the growth rate of larvae reared on a rich diet is particularly accelerated relative to that of larvae reared on a poor diet during the second and third instars. High growth rates during the later stages of larval development suggest that this may be an important stage for investment in adult morphology via resource allocation to imaginal discs, as occurs in other species (Moczek and Nijhout 2004). Because T. angusticollis adults are sexually dimorphic in body size (with males larger, on average, than females) when reared on nutrient-rich larval diets (Bonduriansky 2007), the growth rate of male larvae may be more sensitive to nutrient abundance than the growth rate of female larvae, and the diet effect on mean growth rate may thus be driven by male responses. ...
Nutrient abundance during development has profound effects on adult morphology, life history and behaviour in many insects, but effects of nutrition on juvenile development are less well known. We investigated how larval diet quality affects patterns of growth, development and survival of larvae and pupae in the neriid fly Telostylinus angusticollis (Enderlein). We reared flies on two larval diets varying in nutrient concentration (‘rich’ versus ‘poor’) that have been shown previously to affect a wide range of adult traits in this species. We found that nutrient concentration affected larval growth trajectories, with individuals reared on the rich diet exhibiting greatly accelerated growth and reaching a larger body size. By contrast, we found no evidence that diet affected timing of development at the pupal stage, suggesting that developmental constraints may prevent variation in pupal development rate. Although overall mortality during the immature stages was not affected by larval diet, we found some evidence that individuals reared on a poor diet might experience higher larval mortality, whereas individuals reared on a rich diet might experience higher mortality during emergence from the puparium. Our results enhance understanding of the effects of nutrition on growth, development, and life history.
... (Kawano, 1995), stag beetles (Kawano, 1997) and dung beetles Onthophagus spp. (Emlen, 2001;Moczek & Nijhout, 2004), this and other recent studies have shown that resource trade-off is not a universal trend among animals with sexually selected weapons and ornaments (McCullough & Emlen, 2013;Painting & Holwell, 2013;Schwab & Moczek, 2014). ...
Exaggerated sexually selected traits are assumed to decrease the mobility of bearers. However, previous empirical studies have often failed to support this assumption, possibly because locomotor performance represents the integration of numerous morphological, physiological and behavioural traits. Males of a flower beetle Dicronocephalus wallichii Pouillaude 1914 (Coleoptera: Scarabaeidae: Cetoniinae) possess elongated forelegs and a pair of exaggerated horns, which are used as dual weapons in male–male competition for mates. We investigated whether these two sexual traits impede the maximum sprint speed on bamboo branches with different angles and thicknesses under laboratory conditions. Our results suggested that no negative relationship exists between relative foreleg length or horn length and sprint speed. Elongated forelegs and horns may entail negligible locomotor costs. Males with longer horns and forelegs were found to have longer midlegs and hindlegs independent of body size. Thus, elongated midlegs and hindlegs in males may enhance balance, stabilize running on bamboo branches and compensate for the locomotor costs of bearing exaggerated weapons. Furthermore, a positive relationship was found between horn length and sprint speed on a horizontal branch. Males with longer horns probably have more energy and/or invest more heavily in appendage musculature. As is known in other animals, male horns of D. wallichii may act as honest indicators of body condition.
... Differences in dung preference for breeding and feeding could be driven by increased ❖ www.esajournals.org resource selectivity for the formation of brood balls where dung quality is of high importance (Shafiei et al. 2001, Moczek and Nijhout 2004, Arellano et al. 2015. This is relevant for the construction of interaction networks: by burying dung, rather than just feeding on the liquid component, the breeding networks represent the ecosystem function contributions of dung beetles to a greater extent than feeding networks. ...
Loss of large‐bodied mammals across the globe through hunting, habitat degradation, and fragmentation is one of the most significant anthropogenic impacts on the environment. Cascading effects of these extinctions through ecosystems have been little studied, although correlative studies have revealed co‐extinctions in closely linked groups, with implications for ecosystem structure and function. Despite playing important roles in seed dispersal and hence seedling recruitment, mammals have been largely neglected in network studies. Similarly, the role of secondary seed dispersers, such as ants and dung beetles, has been largely unexplored. Most dung beetles rely on mammal feces for feeding and breeding and provide a suite of important ecosystem functions and services. While dung beetle community responses to environmental change have been widely investigated, studies quantifying the network of associations between dung beetle and mammal species are lacking. By developing the first quantitative mammal–dung beetle networks, we address several important knowledge gaps contributing to the understanding of how interactions in networks involving mammals and secondary insect seed dispersers are structured. We use the resulting quantitative interaction networks to model mammal species extinction scenarios to further explore the consequences for dung beetle populations, and the extent to which networks change the strength of interactions through resource switching. Dung beetle feeding and breeding networks did not differ significantly in structure and showed high nestedness and low levels of trophic specialization. Simulations suggested that mammal extinction scenarios based on mammal body mass and mammal dung volume will impact dung beetle populations to a greater extent than random scenarios of mammal loss. Thus, despite their generalist feeding preferences, realistic mammal extinction scenarios have the potential to negatively impact the dung beetle community, which may have consequences for ecosystem functioning.
... Honesty in sexually selected weapons can be maintained through several mechanisms, including exquisite sensitivity to stress [74], parasite load [75,76], environmental condition [77], and intrinsic cost associated large structures [78,79]. The latter is particularly relevant to weapon systems where large, conspicuous structures often hinder the animals that bear them [80][81][82][83][84][85]. When present, the costs of sexually selected weapons typically increase with trait size, so only the largest animals can develop and wield large weapons and high quality signals are restricted to high quality males [28,78,79,86]. ...
The size of sexually selected weapons and their performance in battle are both critical to reproductive success, yet these traits are often in opposition. Bigger weapons make better signals. However, due to the mechanical properties of weapons as lever systems, increases in size may inhibit other metrics of performance as different components of the weapon grow out of proportion with one another. Here, using direct force measurements, we investigated the relationship between weapon size and weapon force production in two hindleg weapon systems, frog-legged beetles (Sagra femorata) and leaf-footed cactus bugs (Narnia femorata), to test for performance tradeoffs associated with increased weapon size. In male frog-legged beetles, relative force production decreased as weapon size increased. Yet, absolute force production was maintained across weapon sizes. Surprisingly, mechanical advantage was constant across weapon sizes and large weaponed males had disproportionately large leg muscles. In male leaf-footed cactus bugs, on the other hand, there was no relationship between weapon size and force production, likely reflecting the importance of their hindlegs as signals rather than force-producing structures of male-male competition. Overall, our results suggest that when weapon force production is important for reproductive success, large weaponed animals may overcome mechanical challenges by maintaining proportional lever components and investing in (potentially costly) compensatory mechanisms.
... This is in contrast to other dung beetle taxa such as Onthophagus, where male morphs can exhibit marked differences both in head and pronotum morphology [27,28]. Although it is not clear why dimorphic males resemble each other in their head shape patterns, anatomical structures, such as horns, can certainly develop in tandem with more distant body parts if there is a functional aspect involved [58,59]. It is likely that these pronotal shape differences are functionally related to intrasexual competition among C. lunaris males during the breeding season. ...
Male horn dimorphism is a rather common phenomenon in dung beetles, where some adult individuals have well-developed head horns (i.e., major males), while others exhibit diminished horn length (i.e., minor males). We focused on horn dimorphism and associated head and pronotum shape variations in Copris lunaris. We examined the allometric relationship between horn length (i.e., cephalic and pronotal horns) and maximum pronotum width (as index of body size) by fitting linear and sigmoidal models for both sexes. We then asked whether head and pronotum shape variations, quantified using the geometric morphometric approach, contributed to this allometric pattern. We found that female cephalic and pronotal horn growth showed a typical isometric scaling with body size. Horn length in males, however, exhibited sigmoidal allometry, where a certain threshold in body size separated males into two distinct morphs as majors and minors. Interestingly, we highlighted the same allometric patterns (i.e., isometric vs. sigmoidal models) by scaling horn lengths with pronotum shape, making evident that male horn dimorphism is not only a matter of body size. Furthermore, the analysis of shape showed that the three morphs had similar heads, but different pronota, major males showing a more expanded, rounded pronotum than minor males and females. These morphological differences in C. lunaris can ultimately have important functional consequences in the ecology of this species, which should be explored in future work.
... To test these predictions, we compared patterns of genital variation of both shape and relative size to the corresponding patterns of variation in fore-tibiae and heads in the dung beetle genus Onthophagus, an increasingly recognized study system for the evolution and development of insect genitalia (e.g., Palestrini et al. 2000;House and Simmons 2003, 2006, 2007Moczek and Nijhout 2004;Pizzo et al. 2006aPizzo et al. , 2006bPizzo et al. , 2008Pizzo et al. , 2011Pizzo et al. , 2012Simmons and Emlen 2006;Parzer and Moczek 2008;Werner and Simmons 2008;Simmons et al. 2009;Macagno et al. 2011a;Macagno et al. 2011b;Simmons and Garcia-Gonzales 2011;Snell-Rood and Moczek 2012). Even though Onthophagus species can often be distinguished based on external morphological traits, in particular male secondary sexual traits like horns, a large number of species can only be reliably distinguished based on male genitalia (wellstudied examples from just the Mediterranean include five species within the ovatus group (Piera and Zunino 1986), the fracticornis-similis-opacicollis and vacca complex (Macagno et al. 2011b;Roessner et al. 2010); and the sister species O. taurus and O. illyricus, which were also used in this study (see below and Pizzo et al. 2006b)). ...
Insects show relatively little genital variation within species compared to extraordinary and often rapid diversification among species. It has been suggested that selection for reproductive isolation through differences in genital shape might explain this phenomenon. This hypothesis predicts that populations diverge faster in genital shape than in genital size. We tested this prediction in males from 10 dung beetle species with known phylogenetic relationships from the genus Onthophagus (Coleoptera: Scarabaeidae), including four species for which we were able to sample multiple populations. Specifically, we compared intra- and interspecific differentiation in shape and relative sizes of genitalia and calculated their respective evolutionary rates. We compared these rates to two similarly sized non-genital traits, the head and the fore-tibia. We found significant intraspecific variation in genital shape in all four species for which multiple populations were sampled, but for three of them we also identified significant relative size variation. We also found that genital shape evolved at higher rates than relative genital size. Genital shape evolved faster than head shape, but not fore-tibia shape. However, shapes of all measured structures evolved faster than their relative size. We discuss the functional constraints that may bias the developmental evolution of relative size and shape of genitalia and other morphological traits.
... In many cases, organisms can resolve this conflict by linking the expression of sexually dimorphic traits to other cues, such as organism condition [8]. By using organism condition to regulate the expression of the more exaggerated sexually dimorphic structures, organisms can not only reduce the genetic cost of the trait, but also the physiological cost [9], as many of these structures are energetically expensive to produce and maintain [10][11][12][13], but see [14][15][16]. Thus, by regulating the expression of sexually dimorphic traits through both sex-specific loci and the use of conditiondependent plasticity, organisms can achieve the best of both worlds -that is, they ensure that the strongest, healthiest organisms display the most prominently dimorphic structures [8,9] and they reduce the cost of these traits in the opposite sex. ...
Many traits that are sexually dimorphic, appearing either differently or uniquely in one sex, are also sensitive to an organism's condition. This phenomenon seems to have evolved to limit genetic conflict between traits that are under different selective pressures in each sex. Recent work has shed light on the molecular and developmental mechanisms that govern this condition sensitive growth, and this work has now expanded to encompass both sexual dimorphism as well as conditionally plastic growth, as it seems the two phenomena are linked on a molecular level. In all cases studied the gene doublesex, a conserved regulator of sex differentiation, controls both sexual dimorphism as well as the condition-dependent plastic responses common to these traits. However, the advent of next-generation -omics technologies has allowed researchers to decipher the common and diverged mechanisms of sexually dimorphic plasticity and expand investigations beyond the foundation laid by studies utilizing beetle weapons.
... Genetics, hormonal interactions and availability of food resources for the development of exaggerated traits and supporting structures (e.g. other body structures that increase in order to support the presence of exaggerated structures) may be responsible for the change in allometric slope (Eberhard 1982;Emlen and Nijhout 2001;Emlen and Allen 2004;Moczek and Nijhout 2004;Nijhout 1994;Painting and Holwell 2013;Romiti et al. 2015). Considering the sexual dimorphism observed in M. asper, more resources seem to be invested in anterior body parts and antennal length to increase males fitness. ...
The longhorn beetle Morimus asper exhibits the typical sexual dimorphism of cerambycid beetles: males have longer antennae than females and the antennal length also varies greatly among males of the same population. This study explores the sexual dimorphism in M. asper and the scaling relationship between antennal length and body size in males. Our aim was to assess the allometric pattern of these two traits and their potential effects on individual eco-ethological features. Sexual dimorphism was observed in antennal length and in other morphological traits: males showed longer pronota and females larger and longer elytra, suggesting that males allocate more resources to the anterior body traits, while in females more resources are invested in the development of post-prothoracic body traits. The allometric relationship between antennal length and elytra length of males was best described by a segmented regression, which identified a switch point dividing the male population into two different groups. The analysis of covariance showed that smaller males (with elytra length below the switch point) exhibit a positive allometry, while larger males (above the switch point) showed isometric scaling relationship. Our findings showed that morphometric traits were correlated with aspects of male behaviour and ecology: larger males were more frequently found mating, probably because they have an advantage in defending mates and in winning fights against other males.
... The patterns of selection observed here suggest that costs (i.e., limits to fitness resulting from large traits) may offset the benefits of the biggest weapons ( Fig. 2: red arrows). The costs of bearing sexually selected traits have been demonstrated repeatedly (Moczek and Nijhout 2004;Simmons and Emlen 2006;Allen and Levinton 2007;Clark and Dudley 2009;but see McCullough and Emlen 2013), and theory predicts ornaments and weapons should be costly (Zahavi 1975;Iwasa et al. 1991;Biernaskie et al. 2014). ...
Biologists have been fascinated with the extreme products of sexual selection for decades. However, relatively few studies have characterized patterns of selection acting on ornaments and weapons in the wild. Here, we measure selection on a wild population of weapon-bearing beetles (frog legged leaf beetles: Sagra femorata) for two consecutive breeding seasons. We consider variation in both weapon size (hindleg length), and in relative weapon size (deviations from the population average scaling relationship between hindleg length and body size), and provide evidence for directional selection on weapon size per se and stabilizing selection on a particular scaling relationship in this population. We suggest that whenever growth in body size is sensitive to external circumstance such as nutrition, then considering deviations from population-level scaling relationships will better reflect patterns of selection relevant to evolution of the ornament or weapon than will variation in trait size per se. This is because trait-size versus body-size scaling relationships approximate underlying developmental reaction norms relating trait growth with body condition in these species. Heightened condition-sensitive expression is a hallmark of the exaggerated ornaments and weapons favored by sexual selection, yet this plasticity is rarely reflected in the way we think about – and measure – selection acting on these structures in the wild. This article is protected by copyright. All rights reserved
... The expression and maintenance of traits involved in postmating competition (as it occurs in those involved in competition for mating) are energy-and time-consuming (e.g., Moczek and Nijhout 2004). Since the amount of energy that a male can allocate to those traits is finite, recent theoretical models predict that investment in postcopulatory traits should limit investment in traits that enhance premating competitive success (Parker et al. 2013). ...
One paradoxical finding in some mammals is the presence of male-male intrasexual competition in the absence of sexual size dimorphism. It has been a major goal of evolutionary biologists for over a century to understand why some species in which large males can monopolize multiple mates while excluding smaller competitors, exhibit little or no sexual dimorphism. In this paper I examine three of the main hypotheses that have been proposed to explain this conundrum using as study case the Heteromyidae, a rodent family with subtle sexual size dimorphism. Using a phylogenetic comparative approach, I address the potential influence of i) fecundity selection, ii) covariation between pre- and post-copulatory traits, and iii) environmental constraints (resource shortage) in explaining patterns of body size and sexual size dimorphism (SSD) across 62 heteromyid species. Baculum size, a proxy of the strength of post-copulatory sexual selection, and SSD were negatively correlated suggesting that heteromyid rodents balance their reproductive investment between pre- and post-copulatory traits, which may prevent the evolution of extensive SSD. Results also support a role for resource competition in moderating SSD. The amount of SSD correlated negatively with latitude. This can be explained if high productivity relaxes the level of intrasexual competition among females, leading to more male-biased dimorphism since forces acting on both sexes are not cancelled. In line with this argument, territorial species exhibited a higher dimorphism in comparison with social species. No support was found for the fecundity selection hypothesis. Overall, this study provides insight into the factors driving observed patterns of sexual dimorphism in this iconic group and highlights the need to consider a broader framework beyond sexual selection for better understanding the evolution of dimorphism in this family. Keywords: body size, comparative method, kangaroo rat, sexual selection, SSD.
Darwin’s fifth chapter, “The Laws of Variation,” may stand in the shadow of the first four that climax with his presentation of “Natural Selection,” but its importance should not be underestimated. It deals with philosophical and methodological issues in the study of variation that would be hotly debated for decades after the publication of the book, many of which are still unsettled today. As the chapter title suggests, Darwin felt that a proper scientific study of variation had to discover the laws of nature that governed it. He could not simply let it be random. He looked for laws in the patterns of co-occurrence of changes in different parts of the body or the same part in different species and also in the apparent consistencies in the effects of environment and habit. There is no one main line of argument in this chapter, but rather an exploration of multiple possible conceptions, patterns, and laws of variation—all ways in which variation might not be entirely random. For example: To what extent was variation responsive to environmental changes or to the organism’s needs and habits? And if Darwin admitted such responses, then how was his theory any different from Lamarck’s? Do all parts of the organism vary freely and independently or are there hidden connections, correlations, or trade-offs between varying parts of the body? Why do related species seem often to vary in similar ways? Many of these questions are still with us, in modern evolutionary developmental biology (“evo-devo”) and studies of epigenetics.
Evolutionary theory suggests that individuals should express costly traits at a magnitude that optimizes the trait bearer’s cost-benefit difference. Trait expression varies across a species because costs and benefits vary among individuals. For example, if large individuals pay lower costs than small individuals, then larger individuals should reach optimal cost-benefit differences at greater trait magnitudes. Using the cavitation-shooting weapons found in the big claws of male and female snapping shrimp, we test whether size- and sex-dependent expenditures explain scaling and sex differences in weapon size. We found that males and females from three snapping shrimp species (Alpheus heterochaelis, Alpheus angulosus, and Alpheus estuariensis) show patterns consistent with tradeoffs between weapon and abdomen size. For male A. heterochaelis, the species for which we had the greatest statistical power, smaller individuals showed steeper tradeoffs. Our extensive dataset in A. heterochaelis also included data about pairing, breeding season, and egg clutch size. Therefore, we could test for reproductive tradeoffs and benefits in this species. Female A. heterochaelis exhibited tradeoffs between weapon size and egg count, average egg volume, and total egg mass volume. For average egg volume, smaller females exhibited steeper tradeoffs. Furthermore, in males but not females, large weapons were positively correlated with the probability of being paired and the relative size of their pair mates. In conclusion, we identified size-dependent tradeoffs that could underlie reliable scaling of costly traits. Furthermore, weapons are especially beneficial to males and burdensome to females, which could explain why males have larger weapons than females.
Contests are an important aspect of the lives of diverse animals, from sea anemones competing for space on a rocky shore to fallow deer stags contending for access to females. Why do animals fight? What determines when fights stop and which contestant wins? Addressing fundamental questions on contest behaviour, this volume presents theoretical and empirical perspectives across a range of species. The historical development of contest research, the evolutionary theory of both dyadic and multiparty contests, and approaches to experimental design and data analysis are discussed in the first chapters. This is followed by reviews of research in key animal taxa, from the use of aerial displays and assessment rules in butterflies and the developmental biology of weapons in beetles, through to interstate warfare in humans. The final chapter considers future directions and applications of contest research, making this a comprehensive resource for both graduate students and researchers in the field.
Contests are an important aspect of the lives of diverse animals, from sea anemones competing for space on a rocky shore to fallow deer stags contending for access to females. Why do animals fight? What determines when fights stop and which contestant wins? Addressing fundamental questions on contest behaviour, this volume presents theoretical and empirical perspectives across a range of species. The historical development of contest research, the evolutionary theory of both dyadic and multiparty contests, and approaches to experimental design and data analysis are discussed in the first chapters. This is followed by reviews of research in key animal taxa, from the use of aerial displays and assessment rules in butterflies and the developmental biology of weapons in beetles, through to interstate warfare in humans. The final chapter considers future directions and applications of contest research, making this a comprehensive resource for both graduate students and researchers in the field.
Environment-responsive development contributes significantly to the phenotypic variation visible to selection and as such possesses the potential to shape evolutionary trajectories. However, evaluation of the contributions of developmental plasticity to evolutionary diversification necessitates an understanding of the developmental mechanisms underpinning plastic trait expression. We investigated the role of serotonin signaling in the regulation and evolution of horn polyphenism in the beetle genus Onthophagus. Specifically, we assessed the role of serotonin in development by determining whether manipulating serotonin biosynthesis during the larval stage alters body size, developmental rate, and the formation of relative adult trait size in traits characterized by minimal (genitalia), moderate (elytra), and pronounced (horns) nutrition-responsive development in O. taurus. Second, we assessed serotonin's role in evolution by replicating a subset of our approaches across four species reflecting ancestral as well as derived conditions. Lastly, we employed immunohistochemical approaches to begin assessing whether serotonin may be acting via the endocrine or nervous system. Our results show that pharmacological manipulation of serotonin signaling affects overall size, developmental rate, and the body size threshold separating alternate male morphs. Threshold body sizes were affected across species, regardless of the severity of horn polyphenism, and independent of the precise morphological location of horns. However, histological assessments suggest it is unlikely serotonin functions as a neurotransmitter and instead may rely on other mechanisms that remain to be identified. We discuss the most important implications of our results for our understanding of the evolution of and through plasticity in horned beetles and beyond.
Differential growth, the phenomenon where parts of the body grow at different rates, is necessary to generate the complex morphologies of most multicellular organisms. Despite this central importance, how differential growth is regulated remains largely unknown. Recent discoveries, particularly in insects, have started to uncover the molecular-genetic and physiological mechanisms that coordinate growth among different tissues throughout the body and regulate relative growth. These discoveries suggest that growth is coordinated by a network of signals that emanate from growing tissues and central endocrine organs. Here we review these findings and discuss their implications for understanding the regulation of relative growth and the evolution of morphology.
Our understanding of the development and evolution of phenotypic plasticity has evolved in the 30 years since the first Dahlem conference on development and evolution. The focus of this review is on the developmental mechanisms that produce alternative and conditional phenotypes in response to environmental signals. The role of environment is a critical factor in evolution, yet environment is almost universally ignored in developmental biology. The effects of environment are most clearly seen in postembryonic development, where the mechanisms by which environmental signals alter developmental trajectories are increasingly well understood. The outcome of altered developmental pathways is what we recognize as phenotypic plasticity. This chapter shows that the developmental mechanisms that produce phenotypic plasticity are diverse and that control resides largely at the physiological level, often via developmental hormones that switch between alternative developmental fates in response to environmental signals. In conclusion this chapters shows how robustness and homeostatic mechanisms are they key to understanding the evolution of conditional traits.
The elaboration of exaggerated, sexually selected weapons and ornaments often comes at a cost to other traits. For instance, by sustaining the growth of an exaggerated weapon during development, shared and limited resources such as morphogens, growth factors, and nutrients may become depleted and limit the size to which other structures can grow. Such interactions are characteristic of resource allocation trade-offs, which can constrain the production of phenotypic variation and bias evolutionary trajectories. Across many species of Onthophagus beetles, males produce extravagant horns that are used as weapons in male–male competition over mates. Previous studies have reported resource allocation trade-offs between horns and both proximally and distally developing structures. However, more recent studies have largely failed to recover these patterns, leading to the hypothesis that trade-offs may manifest only in certain species, populations, or environmental conditions. Here, we investigate (i) patterns of resource allocation into horns, eyes, and genitalia in Onthophagus gazella and O. taurus, and assess (ii) how these patterns of resource allocation are influenced by nutrient stress during larval development. We find that nutrient stress alters patterns of resource allocation within and among traits, but recover a trade-off only in the species that invests most heavily into horn production (O. taurus), and in individuals of that species that invested a disproportionately large or small amount of resources into horn growth. These results suggest that resource allocation trade-offs may not be as prevalent as previously described, and that their presence and magnitude may instead be highly context dependent.
It is well known that sexual selection can target reproductive traits during successive pre- and post-mating episodes of selection. A key focus of recent studies has been to understand and quantify how these episodes of sexual selection interact to determine overall variance in reproductive success. In this paper we review empirical developments in this field but also highlight the considerable variability in patterns of pre- and post-mating sexual selection, attributable to variation in patterns of resource acquisition and allocation, ecological and social factors, genotype-by-environment interaction, and possible methodological factors that might obscure such patterns. Our aim is to highlight how (co)variances in pre- and post-mating sexually selected traits can be sensitive to changes in a range of ecological and environmental variables. We argue that failure to capture this variation when quantifying the opportunity for sexual selection may lead to erroneous conclusions about the strength, direction or form of sexual selection operating on pre- and post-mating traits. Overall, we advocate for approaches that combine measures of pre- and post-mating selection across contrasting environmental or ecological gradients to better understand the dynamics of sexual selection in polyandrous species. We also discuss some directions for future research in this area. This article is protected by copyright. All rights reserved.
Allometries among body parts of adult holometabolous insects differ from allometries among body parts of many other animals because adult structures (many of which are derived from imaginal disks) do not grow synchronously with the body. Imaginal structures grow little during larval life but experience most of their growth during the prepupal and pupal period, after food intake and somatic growth have ceased. Growth of imaginal tissues thus occurs in a closed system at the expense of nutrients accumulated during larval life. In a closed system, growing imaginal tissues compete for available nutrients, and the growth trajectory and final size of one tissue (or disk) are influenced by the growth of others. We use the Gompertz growth equation and a model of growth in a closed system in which imaginal disks compete for nutrients to model the growth of imaginal disks and the resulting allometric relations among them. By incorporating known features of ant caste development, such as reprogramming of the critical size for metamorphosis in major workers (soldiers) and reprogramming of developmental parameters in individuals larger than a critical size, we show that the nonlinear and discontinuous allometries of ants with polymorphic castes result from normal developmental processes during the metamorphosis of holometabolous insects. The imaginal disk competition model predicts that when one disk is reprogrammed, others will show a compensatory response. Such correlated developmental responses may play a role in the evolution of body proportions in ants, rhinoceros beetles, and other insects.
Polyphenic development is thought to play an important role in the evolution of phenotypic diversity and morphological novelties, yet the evolution of polyphenisms has rarely been docu- mented in natural populations. Here we compare the morphologies of male dung beetles (Onthophagus taurus; Coleoptera: Scarabaeidae) from populations introduced to Australia and the eastern United States. Males in this species express two alternative morphologies in response to larval feeding conditions. Males encountering favourable conditions grow larger than a threshold body size and develop a pair of horns on their heads, whereas males that encounter poor conditions do not reach this threshold size and remain hornless. Australian and US populations did not differ in overall body size ranges, but exhibited significant differences in the location of the critical body size threshold that separates alternative male morphs. Australian males remained hornless at much larger body sizes than males in US populations, resulting in substantial and significant differences in the average body size-horn length allometry between exotic populations, as well as significant differences in morph ratios. The phenotypic divergence observed between field populations was maintained in laboratory populations after two generations under identical environmental conditions, suggesting a genetic basis to allometric divergence in these populations. Divergence between exotic O. taurus populations was of a magnitude and kind typically observed between species. We use our results to examine potential causes of allometric divergence in onthophagine beetles, and discuss the evolutionary potential of threshold traits and polyphenic development in the origin of morphological and behavioural diversity.
Compared reproductive behavior of horned and hornless male dung beetles. Horned males assisted mates in gathering larval provisions and guarded mates' burrows when vacated. Hornless males did not help females during oviposition. Differences in courtship behavior between males indicated that horned males may be assessing female size and employing precopulatory mate discrimination. In the laboratory, hornless males inseminated females on the 1st encounter more often than horned males and exercised minimal mate discrimination. Males' mating frequencies may be different in the field as a result of either intrasexual selection or female choice. Features of mating were the males' tactile stimulation of the female and upward jerks of the head and pronotum before, during, and after copulation. This latter action facilitated dissemination of pheromones from exocrine glands on males' forelegs. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
Changes in form during ontogeny and evolution depend in large measure on changes in the relative growth of the various parts of the body. The current consensus in developmental biology is that the final size of appendages and internal organs is regulated autonomously, within the structure itself. Size regulation of body parts typically requires no external control and is thought to be relatively insensitive to signals from the developmental environment. We show in two very different systems, butterfly wings and beetle horns, that experimentally induced changes in the allocation of developmental resources to one trait produces compensatory changes in the relative sizes of other traits. These findings illustrate that interaction among body parts in development is part of the mechanism of size regulation of those parts. Furthermore, in the case of beetle horns, we show that the tradeoff in size is manifest as a significant negative genetic correlation among the involved body parts and, therefore, constitutes a developmental source of genetic constraint on the evolution of body form.
Reproductive strategies often consist of two alternative tactics whereby males either compete for and guard females, or sneak copulations. By their nature, alternative tactics expose males to differing risks of sperm competition; sneaks will always be subject to sperm competition but guards will be subject to sperm competition with low probability, dependent on the number of sneaks. Recent game-theoretical models predict that males in the sneak role should have the greater gametic expenditure but that the disparity in expenditure should decrease with increasing numbers of sneaks. Male dung beetles in the genus Onthophagus can be separated into two morphs: major males have horns and guard females whereas minor males are hornless and sneak copulations. Here we compare testis size and ejaculate characteristics between these alternative morphs. We find that in O. binodis 30% of males are sneaks, and sneaks have larger testes, ejaculate volumes, and longer sperm than guards. In O. taurus 60% of males are sneaks and there are no differences in gametic traits. Our data thus provide empirical support for game-theoretical models of sperm competition.
Fluctuating asymmetry is often used as a measure of developmental instability, although its developmental basis is poorly understood. Theoretical models and experimental studies have suggested that feedback interactions between structures on the left and right body sides play a pivotal role in the control of asymmetry. Here we provide experimental evidence that competition for a limiting resource can generate such interactions between growing organs. In our experiments in the butterfly Precis coenia (Lepidoptera: Nymphalidae), hindwing imaginal discs were removed from one or both body sides of caterpillars. Emerging butterflies were thus missing one or both hindwings, but had heavier forewings, mid- and hindlegs than untreated controls. When only one hindwing was removed, the forewing and hindleg on the treated side were heavier than on the untreated side. The asymmetry and overall weight increase in response to wing disc removal diminished with increasing physical distance of the responding tissue from the imaginal disc removed. Our findings are consistent with the hypothesis that growing imaginal discs compete for a haemolymph-borne resource, such as a nutrient or growth factor. Such competition is a possible mechanism for feedback interactions and may thus participate in the developmental control of asymmetry.
Darwin considered the horns of male beetles to be among the most striking examples of sexual selection. As with antlers in deer or elk, beetle horns scale positively with male body size, with the result that large males have disproportionately longer horns than small males. It is generally assumed that such scaling relationships ('static allometries') are insensitive to short-term changes in the environment, and for this reason they are regularly used as diagnostic attributes of populations or species. Here I report breeding experiments on horned beetles that demonstrate that the scaling relationship between male horn length and body size changes when larval nutrition changes. Males reared on a low-quality diet had longer horn lengths at any given body size than sibling males reared on a high-quality diet. Such 'allometry plasticity' may explain seasonal changes observed in this same scaling relationship in a natural population. These experiments demonstrate that scaling relationships of sexually selected traits can respond facultatively to variation in the environment, thereby revealing a new mechanism by which males regulate the production of exaggerated secondary sexual traits.
I quantitatively analyzed male morphology of two closely related rhinoceros beetles species (Chalcosoma caucasus F. and Chalcosoma atlas L.) in 12 allopatric and seven sympatric locations throughout Southeast Asia. The qualitative features and the magnitude of intraspecific variation of each species were unaltered between allopatric and sympatric locations. Across allopatric locations, body size, horn size, dimorphic dimension, and genitalia size nearly completely overlapped between C. caucasus and C. atlas. Yet, in all sympatric locations, the differences between the two species in these characters were highly significant. While the enlarged difference between the two species in body size in sympatry could be attributed to habitat differentiation, that in genitalia size far exceeded what was expected from the general body-size displacement. These results indicate that morphological character displacement in sympatry was most complete in sexual organs. This may account for the process of existing species conserving themselves as integrated units by avoiding interspecific competition and enhancing reproductive isolation.
By fractionating conditioned medium (CM) from Drosophila imaginal disc cell cultures, we have identified a family of Imaginal Disc Growth Factors (IDGFs), which are the first polypeptide growth factors to be reported from invertebrates. The active fraction from CM, as well as recombinant IDGFs, cooperate with insulin to stimulate the proliferation, polarization and motility of imaginal disc cells. The IDGF family in Drosophila includes at least five members, three of which are encoded by three genes in a tight cluster. The proteins are structurally related to chitinases, but they show an amino acid substitution that is known to abrogate catalytic activity. It therefore seems likely that they have evolved from chitinases but acquired a new growth-promoting function. The IDGF genes are expressed most strongly in the embryonic yolk cells and in the fat body of the embryo and larva. The predicted molecular structure, expression patterns, and mitogenic activity of these proteins suggest that they are secreted and transported to target tissues via the hemolymph. However, the genes are also expressed in embryonic epithelia in association with invagination movements, so the proteins may have local as well as systemic functions. Similar proteins are found in mammals and may constitute a novel class of growth factors.
During the past ten years, significant progress has been made in understanding the basic mechanisms of the development of multicellular organisms. Genetic analysis of the development of Caenorhabditis elegans and Drosophila has unearthed a fruitful number of genes involved in establishing the basic body plan, patterning of limbs, specification of cell fate and regulation of programmed cell death. The genes involved in these developmental processes have been conserved throughout evolution and homologous genes are involved in the patterning of insect and human limbs. Despite these important discoveries, we have learned astonishingly little about one of the most obvious distinctions between animals: their difference in body size. The mass of the smallest mammal, the bumble-bee bat, is 2 g while that of the largest mammal, the blue whale, is 150 t or 150 million grams. Remarkably, even though they are in the same class, body size can vary up to 75-million-fold. Furthermore, this body growth can be finite in the case of most vertebrates or it can occur continuously throughout life, as for trees, molluscs and large crustaceans. Currently, we know comparatively little about the genetic control of body size. In this article we will review recent evidence from vertebrates and particularly from Drosophila that implicates insulin/insulin-like growth factor-I and other growth pathways in the control of cell, organ and body size.
Sexual selection can favor production of extravagant ornaments and weapons in the contest for access to the opposite sex. Existing explanations for the diversity of sexually selected structures focus on reproductive benefits conferred by particular ornament or weapon morphologies. Here, I show that costs of weapon production also may drive patterns of weapon evolution. In beetles, production of horns reduces the size of neighboring morphological structures (antennae, eyes, or wings, depending on the location of the horns), and these tradeoffs reveal unexpected functional associations between ecology and horn morphology. This study illustrates a critical but overlooked role of costs in sexual selection and has implications for understanding the evolution of animal morphology.
Dung beetles of the genus Onthophagus Latreille are used as model systems in behavioral ecology, evolutionary biology, and insect development. In the past, studies on the developmental control of larval and adult form, and studies that seek to integrate development, evolution, and ecology, have been handicapped by experimenters' inability to determine the sex of developing larvae. Here we present a straightforward, reliable, and non-invasive method that permits sexing of Onthophagus Latreille larvae during their early to mid third instar.
Allometric relationships in primary sexual traits (male and female genitalia), secondary sexual traits (male horns and female carinae), and non-sex-related traits (external body traits, epipharynx traits) were studied in the dung beetle Onthophagus taurus. Model II regressions of log-transformed data were used to quantify relationships, with pronotum width as regressor and indicator of overall body size. Slopes (allometric values) for the different trait categories were significantly different, with secondary sexual traits showing the highest values (higher than 1.0), followed by external body traits (slightly lower than 1.00) and epipharynx traits (around 0.2). Primary sexual traits and body size were mostly uncorrelated and genital sizes were virtually constant. Allometries of secondary sexual traits were quite different in the two sexes: the relationship between male horn length and pronotum width was approximately sigmoidal, while that between female carina length and pronotum width was linear. External body traits had significantly higher allometric values in females than in males. Our results suggest that traits in the different categories are under different kinds of selection. Genital allometries can be explained on the basis of sexual selection by cryptic female choice or by the lock-and-key hypothesis. Among secondary sexual characters, male horn morphology seems to be mostly "environmentally" determined and sexual selection would affect only a component of the developmental mechanism of horn expression. External body characters are likely under natural selection, even though a few traits could be sex-related. Finally, in both sexes, internal epipharynx traits seem to be subject to the same selective pressure, probably because males and females use the same feeding niche. The constancy of genital sizes in O. taurus suggests that in developmental processes, more is invested in primary sexual traits (to produce genitalia of the proper size) than in secondary sexual or body traits. Males receiving low quantities of food may incur costs associated with a small horn or small body size, but do not incur costs associated with small genitalia. Females probably share the same developmental pattern.
Hypotheses regarding the function of elaborate male genitalia were tested in a sample of insects and spiders by comparing their allometric values (slopes in log-log regressions on indicators of body size) with those of other body parts. Male genitalia consistently had lower slopes than other body parts. Perhaps as a consequence of this pattern, genitalic size also tended, though less consistently, to have lower coefficients of variation than did the size of other body parts. The morphological details of coupling between males and females in several species clearly indicated that selection favoring mechanical fit is not responsible for these trends. Sexual selection on male courtship structures that are brought into contact with females in precise ways may favor relatively low allometric values, in contrast to the high values seen in the other sexually selected characters (usually visual display devices) that have been studied previously, because a female's own size will influence her perception of the contact courtship devices of a male.
Males of the horned beetle Onthophagus acuminatus Har. (Coleoptera: Scarabaeidae) exhibit horn length dimorphism due to a sigmoidal allometric relationship between horn length and body size: the steep slope of the allometry around I-he inflection of the sigmoid curve separates males into two groups; those larger than this inflection possess long horns, and those smaller than this inflection have short horns or lack horns. I examined the genetic basis of the allometric relationship between horn length and body size by selecting males that produced unusually long horns, and males that produced unusually short horns, for their respective body sizes. After seven generations of selection, lines selected for relatively long horns had significantly longer horn lengths for a given body size than lines selected for relatively short horns, indicating a heritable component to variation in the allometry. The sigmoidal shape of the allometry was not affected by this selection regime. Rather, selected lines differed in the position of the allometry along the body size axis. One consequence of lateral shifts in this allometric relationship was that the body size separating horned from hornless males (the point of inflection of the sigmoid curve) differed between selection lines: lines in which males were selected for relatively long horns began horn production at smaller body sizes than lines selected for relatively short horns. These results suggest that populations can evolve in response to selection on male horn length through modification of the growth relationship between horn length and body size.
1. Environmental conditions, such as variation in nutrition, commonly contribute to morphological variation among individuals by affecting body size and the expression of certain morphological traits; however the scaling relationship between a morphological trait and body size over a range of body sizes is generally assumed not to change in response to environmental fluctuation (allometric plasticity), but instead to be constant and diagnostic for a particular trait and species or population. The work reported here examined diet‐induced allometric plasticity in the polyphenic beetle Onthophagus taurus Schreber (1759) (Coleoptera: Scarabaeidae).
2. Male O. taurus vary in body size depending on larval nutrition. Only males above a critical body size threshold express fully developed horns; males smaller than this threshold develop only rudimentary horns or no horns at all.
3. Field populations that naturally utilise two different resources for feeding larvae (horse dung vs. cow manure) exhibited significant differences in the average scaling relationship between body size and male horn length over the same range of body sizes. Males collected from cow manure populations expressed consistently longer horns for a given body size than males collected from horse dung populations.
4. Males reared in the laboratory on horse dung or cow manure also exhibited significant differences in the average scaling relationship between body size and horn length. Differences between laboratory populations reared on horse dung or cow manure were of the same kind and magnitude as differences between field populations that utilise these different resources naturally.
5. These findings suggest that between‐population differences in scaling relationships between horn length and body size can be the product of differences in the quality of resources available to developing larvae. Results are discussed in the context of onthophagine mating systems and recent insights in the developmental and endocrine control of horn polyphenisms.
The existence of discrete phenotypic variation within one sex poses interesting questions regarding how such intrasexual polymorphisms are produced and modified during the course of evolution. Approaching these kinds of questions requires insights into the genetic architecture underlying a polymorphism and an understanding of the proximate mechanisms determining phenotype expression. Here we explore the genetic underpinnings and proximate factors influencing the expression of beetle horns – a dramatic sexually selected trait exhibiting intramale dimorphism in many species. Two relatively discrete male morphs are present in natural populations of the dung beetle Onthophagus taurus (Scarabaeidae, Onthophagini). Males exceeding a critical body size develop a pair of long, curved horns on their heads, while those smaller than this critical body size remain essentially hornless. We present results from laboratory breeding experiments designed to assess the relative importance of inherited and environmental factors as determinants of male morphology. Using father–son regressions, our findings demonstrate that horn length and body size of male progeny are not predicted from paternal morphology. Instead, natural variation in an environmental factor, the amount of food available to larvae, determined both the body sizes exhibited by males as adults and the presence or absence of horns. The nonlinear scaling relationship between the body size and horn length of males bred in the laboratory did not differ from the pattern of variation present in natural populations, suggesting that nutritional conditions account for variation in male morphology in natural populations as well. We discuss our results by extending ideas proposed to explain the evolution of conditional expression of alternative phenotypes in physically heterogeneous environments toward incorporating facultative expression of secondary sexual traits. We use this synthesis to begin characterizing the potential origin and subsequent evolution of facultative horn expression in onthophagine beetles.
In a variety of organisms morphological variation is discrete rather than continuous. Discrete variation within a sex has attracted particular interest as it is thought to reflect the existence of alternative adaptations to a heterogeneous selection environment. The beetle Onthophagus taurus shows a dimorphism for male horns: males that exceed a critical body size develop a pair of long, curved horns on their heads, while smaller males remain hornless. In this study we report on the alternative reproductive tactics used by males with these two morphologies, and present experimental and behavioural data suggesting that these alternative tactics selectively favour discretely different male phenotypes. Horned males aggressively defended tunnel entrances containing breeding females. Fights involved the use of horns, and males with longer horns were more likely to win fights. In contrast, hornless males employed nonaggressive sneaking behaviours when faced with competitively superior males. Sneaking behaviours appeared to require high degrees of manoeuvrability inside tunnels to access and mate with females despite the presence of a guarding male. Comparisons of running performances of males with identical body sizes but different horn lengths suggest that the possession of horns reduces male agility inside tunnels. Thus, horn possession confers a clear advantage to males using fighting behaviours to access females, whereas hornlessness may be favoured in males that rely primarily on sneaking behaviours. Combined, the two alternative reproductive tactics used by male O. taurus appear to favour opposite horn phenotypes, which may explain the paucity of intermediate morphologies in natural populations of O. taurus.
Male dung beetles (Onthophagus taurus) facultatively produce a pair of horns that extend from the base of the head: males growing larger than a threshold body size develop long horns, whereas males that do not achieve this size grow only rudimentary horns or no horns at all. Here we characterize the postembryonic development of these beetles, and begin to explore the hormonal regulation of horn growth. Using radioimmune assays to compare the ecdysteroid titers of horned males, hornless males, and females, we identify a small pulse of ecdysteroid which is present in both hornless males and females, but not in horned males. In addition, we identify a brief period near the end of the final (third) larval instar when topical applications of the juvenile hormone analog methoprene can switch the morphology of developing males. Small, normally hornless, males receiving methoprene during this sensitive period were induced to produce horns in 80% of the cases. We summarize this information in two models for the hormonal control of male dimorphism in horn length.
Facultative expression of alternative male morphologies is thought to allow individual males to select the phenotype with the highest fitness gain given their competitive status relative to other males with which they compete for females. Choice of, or switching between, morphs commonly relies on developmental threshold responses. Evolutionary changes in developmental threshold responses are thought to provide an important avenue for phenotypic diversification and the evolution of morphological and behavioral novelties. However, the extent to which alternative male phenotypes and their underlying threshold responses actually evolve in natural populations is unclear. Likewise, the ecological factors that shape the evolution of threshold responses in natural populations are unexplored for most organisms, as are the consequences of such modifications for patterns of morphological diversity. I examined the ecological basis of rapid threshold evolution in exotic populations of the horn-polyphenic dung beetle Onthophagus taurus. Male O. taurus vary continuously in body size as a function of larval feeding conditions. Only males that exceed a critical threshold body size develop a pair of long horns on their heads, whereas males below this threshold remain hornless. Populations in two exotic ranges of this species, the eastern United States and western Australia, have diverged in the mean threshold body size, which has resulted in the evolution of highly divergent and novel horn length--body size allometries in these populations. Populations in a third and previously unstudied exotic range of O. taurus in eastern Australia exhibit threshold body sizes roughly intermediate between the eastern U.S. and western Australian populations. I tested three hypothesis to explain how differences in ecological and demographic factors can drive allometric divergences between populations, using data derived from comparative, standardized sampling of a large number of populations in each exotic range. Results suggest that differences in the intensity of both intra- and interspecific competition have contributed to the evolution of divergent thresholds in these populations. My results do not support the hypothesis that shifts in threshold body sizes to larger body sizes are a consequence of increases in the mean body size of competing males. I discuss my results in the context of Onthophagus mating systems and the evolutionary implications of threshold evolution. Copyright 2003.
Cells employ a diverse array of signaling mechanisms to establish spatial patterns during development. Nowhere is this better understood than in Drosophila, where the limbs and eyes arise from discrete epithelial sacs called imaginal discs. Molecular-genetic analyses of pattern formation have generally treated discs as single epithelial sheets. Anatomically, however, discs comprise a columnar cell monolayer covered by a squamous epithelium known as the peripodial membrane. Here we demonstrate that during development, peripodial cells signal to disc columnar cells via microtubule-based apical extensions. Ablation and targeted gene misexpression experiments demonstrate that peripodial cell signaling contributes to growth control and pattern formation in the eye and wing primordia. These findings challenge the traditional view of discs as monolayers and provide foundational evidence for peripodial cell function in Drosophila appendage development.
Size regulation is fundamental in developing multicellular organisms and occurs through the control of cell number and cell size. Studies in Drosophila have identified an evolutionarily conserved signaling pathway that regulates organismal size and that includes the Drosophila insulin receptor substrate homolog Chico, the lipid kinase PI(3)K (Dp110), DAkt1/dPKB, and dS6K.
We demonstrate that varying the activity of the Drosophila insulin receptor homolog (DInr) during development regulates organ size by changing cell size and cell number in a cell-autonomous manner. An amino acid substitution at the corresponding position in the kinase domain of the human and Drosophila insulin receptors causes severe growth retardation. Furthermore, we show that the Drosophila genome contains seven insulin-like genes that are expressed in a highly tissue- and stage-specific pattern. Overexpression of one of these insulin-like genes alters growth control in a DInr-dependent manner.
This study shows that the Drosophila insulin receptor autonomously controls cell and organ size, and that overexpression of a gene encoding an insulin-like peptide is sufficient to increase body size.
Polyphenic development is thought to play a pivotal role in the origin of morphological novelties. However, little is known about how polyphenisms evolve in natural populations, the developmental mechanisms that may mediate such evolution, and the consequences of such modification for patterns of morphological variation. Here we examine the developmental mechanisms of polyphenism evolution in highly divergent natural populations of the dung beetle, Onthophagus taurus. Males of this species express two alternative morphologies in response to larval feeding conditions. Favorable conditions cause males to grow larger than a threshold body size and to develop a pair of horns on their heads. Males that encounter relatively poor conditions during larval life do not reach this threshold size and remain hornless. Exotic populations of O. taurus have diverged dramatically in body size thresholds in less than 40 years since introduction to new habitats, resulting in the expression of highly divergent and novel horn length-body size scaling relationships in these populations. Here we show that larvae of populations that have evolved a larger threshold body size (1) have to accumulate greater mass to become competent to express the horned morph, (2) require more time to complete the final instar, (3) are less sensitive to the juvenile hormone (JH) analogue methoprene, and (4) exhibit a delay in the sensitive period for methoprene relative to other developmental events. JH has been shown previously to control horn expression in this species. Our results show that threshold evolution may be mediated via changes in the degree and timing of sensitivity to JH and may result in correlated changes in the dynamics and duration of larval development. Strain-specific differences in JH sensitivity have previously been demonstrated in other insects. However, to the best of our knowledge this is the first demonstration that changes in the timing of the sensitive period for JH may play an equally important role in the evolution of novel thresholds. We discuss our findings in the context of the developmental regulatory mechanisms that underlie polyphenic development and use our results to explore the consequences of, and constraints on, polyphenism evolution in nature.
The mechanisms that control the growth rate of internal tissues during postembryonic development are poorly understood. In insects, the growth rate of imaginal disks varies with nutrition and keeps pace with variation in somatic growth. We describe here a mechanism by which the growth of wing imaginal disks is controlled. When wing imaginal disks of the butterfly Precis coenia are removed from the larva and placed in a standard nutrient-rich tissue culture medium they stop growing, suggesting that nutrients alone are not sufficient to support normal growth. Such disks can be made to grow at a normal rate by supplementing the culture medium with an optimal concentration of the steroid hormone 20-hydroxyecdysone and with hemolymph taken from growing larvae. The growth-promoting activity of the hemolymph is caused by a heat-stable factor that can be extracted from the CNS and appears to be identical to the neurohormone bombyxin, a member of the insulin family of proteins. Synthetic bombyxin stimulates growth at concentrations as low as 30 ngml, and specific antibodies to bombyxin completely remove growth-promoting activity from the hemolymph. Bombyxin evidently acts together with 20-hydroxyecdysone to stimulate cell division and growth of wing imaginal disks. It appears that the level of bombyxin in the hemolymph is modulated by the brain in response to variation in nutrition and is part of the mechanism that coordinates the growth of internal organs with overall somatic growth.
Polyphenisms are thought to play an important role in the evolution of phenotypic diversity and the origin of morphological and behavioral novelties. However, the extent to which polyphenic developmental mechanisms evolve in natural populations is unknown. Here we contrast patterns of male phenotype expression in native and exotic and ancestral and descendant populations of the horn polyphenic beetle, Onthophagus taurus. Males in this species express two alternative morphologies in response to larval feeding conditions. Favorable conditions cause males to grow larger than a threshold body size and to develop a pair of horns on their heads. Males that encounter relatively poor conditions do not reach this threshold size and remain hornless. We show that exotic and native populations of O. taurus differ significantly in the body size threshold that separates alternative male phenotypes. Comparison with archival museum collections and additional samples obtained from the native range of O. taurus suggests that allometric differences between exotic and native populations do not reflect preexisting variation in the native range of this species. Instead, our data suggest that threshold divergences between exotic and native populations have evolved in less than 40 years since the introduction to a new habitat and have proceeded in opposite directions in two exotic ranges of this species. Finally, we show that the kind and magnitude of threshold divergence between native and exotic populations are similar to differences normally observed between species. Our results support the view that certain components of the developmental control mechanism that underlie polyphenic development can evolve rapidly in natural populations and may provide important avenues for phenotypic differentiation and diversification in nature. We discuss the role of developmental control mechanisms in the origin of allometric diversification and explore potential evolutionary mechanisms that could drive scaling relationship evolution in nature.
During the last larval instar, the wing imaginal disks of Precis coenia grow continuously. The rate of disk growth is not disk-autonomous but closely matches the rate of somatic growth of the larva, so that the size of the disks is a function of the size of the body, irrespective of the growth rate of the larva. When larvae are starved, their wing disks cease growth within 4 h, which indicates the existence of an efficient coupling mechanism between the growth of the soma and growth of the imaginal disks. Disk growth is inhibited by juvenile hormone in a dose-dependent manner. In the presence of the hormone the wing disks stop growing even while the larva continues to grow normally. During the last larval instar the wing imaginal disks also undergo a complex differentiation, consisting of the development of the lacunae and tracheation that define the future adult wing venation system. In normally growing larvae, differentiation of the wing disk is tightly correlated with wing size. Differentiation and size can be dissociated by starvation. If larvae are starved at any time after differentiation has begun, differentiation continues at a normal rate, even though the wing disk does not grow. Differentiation does not begin spontaneously in larvae that are starved before differentiation has begun. These findings indicate that the initiation of differentiation and its continuation are controlled independently. Juvenile hormone inhibits differentiation in a dose-dependent manner. Upon treatment with juvenile hormone, the stage of differentiation becomes fixed. These findings indicate that continued differentiation of the wing disk can only occur in the absence of juvenile hormone. Although the circulating level of juvenile hormone may be elevated during starvation, it is unlikely that this elevation is responsible for the observed effect of starvation on growth and differentiation of the disk.
Angewandte Statistik
- L Sachs
Sachs, L. 1992. Angewandte Statistik. Springer, Berlin.
- R R Sokal
- F J Rohlf
Sokal, R. R., and F. J. Rohlf. 1995. Biometry. W. H. Freeman, New York.