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Significance Many organisms, from plants to humans, have long evolutionary histories with nematode worms. Historically these relationships have been assumed to be detrimental—as with intestinal or blood-borne parasites—or at best innocuous, to their hosts. However, this paradigm has been challenged recently, for example, with findings in mammals that worms can modulate their host’s immune system and thereby thwart autoimmune disease. In our study, we describe a phenomenon wherein sexually transmitted and parentally provided worms benefit their insect hosts, possibly by “engineering” the microbiome present in the maternally constructed chamber where offspring develop. Given nematodes’ association with many insects, particularly those with parental care, this phenomenon may be a more widespread feature of insect health., A recent accumulation of studies has demonstrated that nongenetic, maternally transmitted factors are often critical to the health and development of offspring and can therefore play a role in ecological and evolutionary processes. In particular, microorganisms such as bacteria have been championed as heritable, symbiotic partners capable of conferring fitness benefits to their hosts. At the same time, parents may also pass various nonmicrobial organisms to their offspring, yet the roles of such organisms in shaping the developmental environment of their hosts remain largely unexplored. Here, we show that the nematode Diplogastrellus monhysteroides is transgenerationally inherited and sexually transmitted by the dung beetle Onthophagus taurus. By manipulating artificial chambers in which beetle offspring develop, we demonstrate that the presence of D. monhysteroides nematodes enhances the growth of beetle offspring, empirically challenging the paradigm that nematodes are merely commensal or even detrimental to their insect hosts. Finally, our research presents a compelling mechanism whereby the nematodes influence the health of beetle larvae: D. monhysteroides nematodes engineer the bacterial and fungal communities that also inhabit the beetle developmental chambers, including specific taxa known to be involved in biomass degradation, possibly allowing larval beetles better access to their otherwise recalcitrant, plant-based diet. Thus, our findings illustrate that nongenetic inheritance can include intermediately sized organisms that live and proliferate in close association with, and in certain cases enhance, the development of their hosts’ offspring.

Sexual dimorphism accounts for a large fraction of intraspecific diversity. However, not all traits are equally sexually dimorphic; instead, individuals are mosaics of tissues that vary in their ability to exhibit dimorphism. Furthermore, the degree of a trait's sexual dimorphism is frequently environment‐dependent, with elaborate sexual dimorphism commonly being restricted to high nutritional conditions. Understanding the developmental basis and evolution of condition‐dependent sexual dimorphism can be critically informed by determining – across tissues and nutritional conditions – what sex‐biased genes are deployed and how they interact and translate into functional processes. Indeed, key theories concerning the evolution of condition‐dependent sexually dimorphic traits rest on assumptions regarding their developmental genetic underpinnings, yet, have largely gone unexamined by empirical studies. Here, we provide such evidence by investigating the transcriptomic basis of tissue‐ and nutrition‐dependent sexual dimorphism in the bull‐headed dung beetle Onthophagus taurus. Our findings suggest (1) that generating morphological sexual dimorphism requires sex‐biased gene expression in and developmental remodeling of both sexes, regardless of which sex exhibits externally visible trait exaggeration, (2) that although sexually dimorphic phenotypes are comprised of traits underlain by independent repertoires of sex‐biased gene expression, they act similarly at a functional level, and (3) that sexual dimorphism and condition‐dependence share common genetic underpinnings specifically in sexually‐selected traits.

The large size and rapid development of amphibian embryos has facilitated ground-breaking discoveries in developmental biology. Here, we describe the embryogenesis of the Budgett's frog (Lepidobatrachus laevis), an unusual species with eggs that are over twice the diameter of laboratory Xenopus, and embryos that can tolerate higher temperatures to develop into a tadpole four times more rapidly. In addition to detailing their early development, we demonstrate that, like Xenopus, these embryos are amenable to explant culture assays and can express exogenous transcripts in a tissue-specific manner. Moreover, the steep developmental trajectory and large scale of Lepidobatrachus make it exceptionally well-suited for morphogenesis research. For example, the developing organs of the Budgett's frog are massive compared to those of most model species, and are composed of larger individual cells, thereby affording increased subcellular resolution of early vertebrate organogenesis. Furthermore, we found that complete limb regeneration, which typically requires months to achieve in most vertebrate models, occurs in a matter of days in the Budgett's tadpole, which substantially accelerates the pace of experimentation. Thus, the unusual combination of the greater size and speed of the Budgett's frog model provides inimitable advantages for developmental studies—and a novel inroad to address the mechanisms of spatiotemporal scaling during evolution.