skip to main content


Title: Evolution and plasticity of morph‐specific integration in the bull‐headed dung beetle Onthophagus taurus
Abstract

Developmental and evolutionary processes underlying phenotypic variation frequently target several traits simultaneously, thereby causing covariation, or integration, among phenotypes. While phenotypic integration can be neutral, correlational selection can drive adaptive covariation. Especially, the evolution and development of exaggerated secondary sexual traits may require the adjustment of other traits that support, compensate for, or otherwise function in a concerted manner. Although phenotypic integration is ubiquitous, the interplay between genetic, developmental, and ecological conditions in shaping integration and its evolution remains poorly understood. Here, we study the evolution and plasticity of trait integration in the bull‐headed dung beetleOnthophagus tauruswhich is characterized by the polyphenic expression of horned (‘major’) and hornless (‘minor’) male morphs. By comparing populations subject to divergent intensities of mate competition, we tested whether mating system shifts affect integration of traits predicted to function in a morph‐specific manner. We focussed on fore and hind tibia morphology as these appendages are used to stabilize major males during fights, and on wings, as they are thought to contribute to morph‐based differences in dispersal behavior. We found phenotypic integration between fore and hind tibia length and horn length that was stronger in major males, suggesting phenotypic plasticity in integration and potentially secondary sexual trait compensation. Similarly, we observed that fore tibiashapewas also integrated with relative horn length. However, although we found population differentiation in wing and tibia shape and allometry, populations did not differ in integration. Lastly, we detected little evidence for morph differences in integration in either tibia or wing shape, although wing allometries differed between morphs. This contrasts with previous studies documenting intraspecific differentiation in morphology, behavior, and allometry as a response to varying levels of mate competition acrossO. tauruspopulations. We discuss how sexual selection may shape morph‐specific integration, compensation, and allometry across populations.

 
more » « less
Award ID(s):
1901680
NSF-PAR ID:
10380377
Author(s) / Creator(s):
 ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Ecology and Evolution
Volume:
10
Issue:
19
ISSN:
2045-7758
Page Range / eLocation ID:
p. 10558-10570
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Sexual selection can lead to rapid evolution of sexual traits and striking morphological diversity across taxa. In populations where competition for mates is intense, males sometimes evolve distinct behavioral strategies along with morphological differences that help them secure mating opportunities. Strong postcopulatory selection and differential resource allocation across male strategy type can result in strategy‐specific differences in sexual traits, such as sperm morphology, ejaculate components, and testis size. Some polymorphic species also have strategy‐specific genital morphology. Thus far, among vertebrates, this has only been observed in fish. Here, we present the first morphological description of the intromittant copulatory organ, the hemipenis, of the three mating types of the side‐blotched lizard,Uta stansburiana, from a population that exhibits alternative mating strategies. We found that the isometrically scaling hemipenis was shortest in the nonterritorial (yellow) morph that sneaks copulations with other males' mates. Although the hemipenes were generally the same shape across morphs, the usurping territorial (orange) morph had a significantly wider apical horn than the nonterritorial sneaker morph. Sneaker males also had smaller relative body masses than both the mate‐guarding (blue) morph and the usurper morph, and shorter tibia than the usurper morph. This study using a small sample of males suggests that strong sexual selection may drive genital trait differentiation across morphs within populations of terrestrial vertebrates.

     
    more » « less
  2. Abstract

    Nutrition-dependent growth of sexual traits is a major contributor to phenotypic diversity, and a large body of research documents insulin signalling as a major regulator of nutritional plasticity. However, findings across studies raise the possibility that the role of individual components within the insulin signalling pathway diverges in function among traits and taxa. Here, we use RNAi-mediated transcript depletion in the gazelle dung beetle to investigate the functions of forkhead box O (Foxo) and two paralogs of the insulin receptor (InR1 and InR2) in shaping nutritional plasticity in polyphenic male head horns, exaggerated fore legs, and weakly nutrition-responsive genitalia. Our functional genetic manipulations led to three main findings: FoxoRNAi reduced the length of exaggerated head horns in large males, while neither InR1 nor InR2 knock-downs resulted in measurable horn phenotypes. These results are similar to those documented previously for another dung beetle (Onthophagus taurus), but in stark contrast to findings in rhinoceros beetles. Secondly, knockdown of Foxo, InR1, and InR2 led to an increase in the intercept or slope of the scaling relationship of genitalia size. These findings are in contrast even to results documented previously for O. taurus. Lastly, while FoxoRNAi reduces male forelegs in D. gazella and O. taurus, the effects of InR1 and InR2 knockdowns diverged across dung beetle species. Our results add to the growing body of literature indicating that despite insulin signalling's conserved role as a regulator of nutritional plasticity, the functions of its components may diversify among traits and species, potentially fuelling the evolution of scaling relationships.

     

    more » « less
  3. Abstract

    Divergence of sexual signals between populations can lead to speciation, yet opportunities to study the immediate aftermath of novel signal evolution are rare. The recent emergence and spread of a new mating song, purring, in Hawaiian populations of the Pacific field cricket (Teleogryllus oceanicus) allows us to investigate population divergence soon after the origin of a new signal. Male crickets produce songs with specialized wing structures to attract mates from afar (calling) and entice them to mate when found (courtship). However, in Hawaii, these songs also attract an eavesdropping parasitoid fly (Ormia ochracea) that kills singing males. The novel purring song, produced with heavily modified wing morphology, attracts female crickets but not the parasitoid fly, acting as a solution to this conflict between natural and sexual selection. We've recently observed increasing numbers of purring males across Hawaii. In this integrative field study, we investigated the distribution of purring and the proportion of purring males relative to other morphs in six populations on four islands and compared a suite of phenotypic traits (wing morphology, calling song and courtship song) that make up this novel signal across populations of purring males. We show that purring is found in varying proportions across five, and is locally dominant in four, Hawaiian populations. We also show that calling songs, courtship songs and wing morphology of purring males differ geographically. Our findings demonstrate the rapid pace of evolution in island populations and provide insights into the emergence and divergence of new sexual signals over time.

     
    more » « less
  4. Abstract

    Many organisms actively manipulate the environment in ways that feed back on their own development, a process referred to as developmental niche construction. Yet, the role that constructed biotic and abiotic environments play in shaping phenotypic variation and its evolution is insufficiently understood. Here, we assess whether environmental modifications made by developing dung beetles impact the environment‐sensitive expression of secondary sexual traits. Gazelle dung beetles both physically modify their ontogenetic environment and structure their biotic interactions through the vertical inheritance of microbial symbionts. By experimentally eliminating (i) physical environmental modifications and (ii) the vertical inheritance of microbes, we assess the degree to which (sym)biotic and physical environmental modifications shape the exaggeration of several traits varying in their degree and direction of sexual dimorphism. We expected the experimental reduction of a larva's ability to shape its environment to affect trait size and scaling, especially for traits that are sexually dimorphic and environmentally plastic. We find that compromised developmental niche construction indeed shapes sexual dimorphism in overall body size and the absolute sizes of male‐limited exaggerated head horns, the strongly sexually dimorphic fore tibia length and width, as well as the weakly dimorphic elytron length and width. This suggests that environmental modifications affect sex‐specific phenotypic variation in functional traits. However, most of these effects can be attributed to nutrition‐dependent plasticity in size and non‐isometric trait scaling rather than body‐size‐independent effects on the developmental regulation of trait size. Our findings suggest that the reciprocal relationship between developing organisms, their symbionts, and their environment can have considerable impacts on sexual dimorphism and functional morphology.

     
    more » « less
  5. Abstract

    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 genusOnthophagus. Specifically, we assessed the role of serotonin indevelopmentby 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 inO. taurus. Second, we assessed serotonin's role inevolutionby 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.

     
    more » « less