Insights into how development and life-history dynamics shape the evolution of venom

Abstract

Venomous animals are a striking example of the convergent evolution of a complex trait. These animals have independently evolved an apparatus that synthesizes, stores, and secretes a mixture of toxic compounds to the target animal through the infliction of a wound. Among these distantly related animals, some can modulate and compartmentalize functionally distinct venoms related to predation and defense. A process to separate distinct venoms can occur within and across complex life cycles as well as more streamlined ontogenies, depending on their life-history requirements. Moreover, the morphological and cellular complexity of the venom apparatus likely facilitates the functional diversity of venom deployed within a given life stage. Intersexual variation of venoms has also evolved further contributing to the massive diversity of toxic compounds characterized in these animals. These changes in the biochemical phenotype of venom can directly affect the fitness of these animals, having important implications in their diet, behavior, and mating biology. In this review, we explore the current literature that is unraveling the temporal dynamics of the venom system that are required by these animals to meet their ecological functions. These recent findings have important consequences in understanding the evolution and development of a convergent complex trait and its organismal and ecological implications.

Keywords: Complex trait; Convergent evolution; Defense; Ontogeny; Predation; Sexual dimorphism; Spatiotemporal gene expression; Toxins.

Fig. 1

The convergent evolution for the separation of venom composition in animals. Lineages with known venomous taxa are depicted in blue. Boxes on branches highlight the evolution of venomous lineages that exhibit venom heterogeneity among morphological (spatial) and cellular structures, life history (temporal), and sexes (intersexual). The spatial separation of venom is predicted according to Table 2 provided in Schendel et al. [10], given evidence of animals that have a morphologically complex venom apparatus and putative multifunctional toxins profiles

Fig. 2

Development of the venom system in the model sea anemone Nematostella vectensis. a The life cycle and timeline of N. vectensis, with a conservative estimate of the occurrence and diversity of venom-secreting cells. The shifting roles of venom across the development of N. vectensis, from being toxic (purple) to having additional defensive (dark green) and predatory (cyan) functions. Schematic representing the minimum number of types of gland cells (red) and nematocytes (green). b–d Immunostaining Nv1 localized in ectodermal gland cells of N. vectensis polyp [69]. e–g Nematocytes from transgenic polyp expressing mOrange2 under control of NEP3 promoter and embedded in the cuticle of Artemia salina. Only one nematocyte in the picture is mOrange2 positive [70]. UE unfertilized eggs, G gastrula, P planula, M metamorphosis, PP primary polyp, AP Adult polyp

Fig. 3

Spatial separation of functionally distinct venom in animals. a Cone snail. b Assassin bug; anterior main gland (AMG), posterior main gland (PMG), accessory gland (AG), and gut (G). c Sea anemone. Predation-evoked venom profile highlighted in cyan and defense-evoked venom highlighted in dark green