Maternal and larval niche construction interact to shape development, survival, and population divergence in the dung beetle<i>Onthophagus taurus</i>

Dury, Guillaume J.; Moczek, Armin P.; Schwab, Daniel B.

doi:10.1111/ede.12348

Cited by 11 publications

(12 citation statements)

References 49 publications

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“…In regard to IGEs and heritability, research on domestic chickens suggests that IGEs could account for up to 87% of heritable variation in survival found in crossbred chickens [24]. For NC, recent experimental studies of maternal and larval NC in dung beetles, show robust influences on offspring traits, fitness and heritability [46][47][48].…”

Section: Discussionmentioning

confidence: 99%

Niche construction in quantitative traits: heritability and response to selection

Fogarty

Wade

2022

Proc. R. Soc. B.

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A central tenet of niche construction (NC) theory is that organisms can alter their environments in heritable and evolutionarily important ways, often altering selection pressures. We suggest that the physical changes niche constructors make to their environments may also alter trait heritability and the response of phenotypes to selection. This effect might change evolution, over and above the effect of NC acting via selection alone. We develop models of trait evolution that allow us to partition the effects of NC on trait heritability from those on selection to better investigate their distinct effects. We show that the response of a phenotype to selection and so the pace of phenotypic change can be considerably altered in the presence of NC and that this effect is compounded when trans-generational interactions are included. We argue that novel mathematical approaches are needed to describe the simultaneous effects of NC on trait evolution via selection and heritability. Just as indirect genetic effects have been shown to significantly increase trait heritability, the effects of NC on heritability in our model suggest a need for further theoretical development of the concept of heritability.

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Section: Discussionmentioning

confidence: 99%

Niche construction in quantitative traits: heritability and response to selection

Fogarty

Wade

2022

Proc. R. Soc. B.

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“…Alternative hypotheses to resource limitation that could affect body size and SSD differences between populations include environmental differences (Dury et al, 2020 ), differences in predation/parasitism (Servín‐Pastor et al, 2021 ), differences in gut microbiota due to differing dung resource (Winfrey & Sheldon, 2021 ), and the possible involvement of cryptic species. Due to the close geographical proximity of peninsular Malaysia and Singapore, most climatic variables such as rainfall and temperature do not significantly differ, with both countries subject to similar patterns of monsoon seasons.…”

Section: Discussionmentioning

confidence: 99%

“…Alternative hypotheses to resource limitation that could affect body size and SSD differences between populations include environmental differences (Dury et al, 2020) (Shafiei et al, 2001). If mothers from SG populations allocate more dung in the construction of male offspring brood balls than that of females, sex-biased differential maternal investment in offspring could be the driving proximate mechanism of male-biased SSD.…”

Section: Sexual Size Dimorphism (Ssd) Varied Among Populationsmentioning

confidence: 99%

“…the most species rich genus in the animal kingdom), have been gaining increased interest as models in evolutionary research. Recent studies show that their morphology and genetic variation can be influenced by sexual selection, parental investment, and environmental variation via a multitude of complex mechanisms (Dury et al, 2020 ; Hu et al, 2020 ; Schwab et al, 2019 ; Snell‐Rood et al, 2016 ). They are particularly popular in sexual selection research because many species display strong sexual dimorphisms (Parzer & Moczek, 2008 ).…”

Section: Introductionmentioning

confidence: 99%

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Sexual size dimorphism and male reproductive traits vary across populations of a tropical rainforest dung beetle species (Onthophagus babirussa)

Toh

Yap

Goh

et al. 2022

Ecology and Evolution

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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.

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“…As the developing larva continually defecates, works its own excrement into the brood ball, and then re-eats the resulting mixture, the maternally inherited gut microbiome is spread throughout the brood ball, thereby increasing its ability to pre-digest macromolecules outside the larval gut, at least as assayed by in vitro studies [7,32]. Experimental withholding of these modifications results in prolonged development, smaller size and reduced secondary sexual trait expression (but see [33]), suggesting that these environmental modification aids in the extraction of nutrients from an otherwise recalcitrant diet and thus feeds back onto larval development [32,34]. The brood ball can thus be regarded as an extended phenotype [35], or as a product of maternal and larval niche construction [36].…”

Section: Introductionmentioning

confidence: 99%

Vertically inherited microbiota and environment modifying behaviours conceal genetic variation in dung beetle life history

Rohner,

Moczek

2024

Proc. R. Soc. B.

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Diverse organisms actively manipulate their (sym)biotic and physical environment in ways that feed back on their own development. However, the degree to which these processes affect microevolution remains poorly understood. The gazelle dung beetle both physically modifies its ontogenetic environment and structures its biotic interactions through vertical symbiont transmission. By experimentally eliminating (i) physical environmental modifications and (ii) the vertical inheritance of microbes, we assess how environment modifying behaviour and microbiome transmission shape heritable variation and evolutionary potential. We found that depriving larvae of symbionts and environment modifying behaviours increased additive genetic variance and heritability for development time but not body size. This suggests that larvae's ability to manipulate their environment has the potential to modify heritable variation and to facilitate the accumulation of cryptic genetic variation. This cryptic variation may become released and selectable when organisms encounter environments that are less amenable to organismal manipulation or restructuring. Our findings also suggest that intact microbiomes, which are commonly thought to increase genetic variation of their hosts, may instead reduce and conceal heritable variation. More broadly, our findings highlight that the ability of organisms to actively manipulate their environment may affect the potential of populations to evolve when encountering novel, stressful conditions.

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Maternal and larval niche construction interact to shape development, survival, and population divergence in the dung beetleOnthophagus taurus

Cited by 11 publications

References 49 publications

Niche construction in quantitative traits: heritability and response to selection

Niche construction in quantitative traits: heritability and response to selection

Sexual size dimorphism and male reproductive traits vary across populations of a tropical rainforest dung beetle species (Onthophagus babirussa)

Vertically inherited microbiota and environment modifying behaviours conceal genetic variation in dung beetle life history

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