Venom Complexity in a Pitviper Produced by Facultative Parthenogenesis

J J Calvete,D R Rokyta,G W Schuett,S Quesada-Bernat,W Wüster,C F Smith,L Sanz,N R Casewell,D Storey,U Hernández-Guzmán,W Booth,L.-O Albulescu

doi:10.1038/s41598-018-29791-y

Abstract

Facultative parthenogenesis (FP) is asexual reproduction in plant and animal species that would otherwise reproduce sexually. This process in vertebrates typically results from automictic development (likely terminal fusion) and is phylogenetically widespread. In squamate reptiles and chondrichthyan fishes, FP has been reported to occur in nature and can result in the production of reproductively viable offspring; suggesting that it is of ecological and evolutionary significance. However, terminal fusion automixis is believed to result in near genome-wide reductions in heterozygosity; thus, FP seems likely to affect key phenotypic characters, yet this remains almost completely unstudied. Snake venom is a complex phenotypic character primarily used to subjugate prey and is thus tightly linked to individual fitness. Surprisingly, the composition and function of venom produced by a parthenogenetic pitviper exhibits a high degree of similarity to that of its mother and conspecifics from the same population. Therefore, the apparent loss of allelic diversity caused by FP appears unlikely to have a significant impact on the prey-capturing ability of this snake. Accordingly, the pitviper offspring produced by FP retained complex phenotypic characteristics associated with fitness. This result reinforces the potential ecological and evolutionary importance of FP and questions our understanding of the inheritance of venom-associated genes.

Highlights

In this study we assess the implications that the dramatic loss of genetic diversity resulting from automictic development might have on free-living parthenogens
Our results demonstrate that the parthenogen exhibits considerable complexity in venom composition, with a wide diversity of venom proteins being detected at varying molecular weights and isoelectric points (Fig. 2A)
To provide a higher resolution analysis, venom proteins found in each of the four venoms were separated using a combination of reverse-phase high-performance liquid chromatography (RP-HPLC) and one-dimensional SDS-PAGE gel electrophoresis of the isolated chromatographic fractions

Summary

Introduction

In this study we assess the implications that the dramatic loss of genetic diversity resulting from automictic development might have on free-living parthenogens. The only studies that report the phenotypic consequences relating to FP in vertebrates have focused on colour and patterns, with parthenogenetic offspring exhibiting homozygosity, regardless of whether that specific trait is inherited recessively or through incomplete dominance[5,15]. In contrast to those previous examples, snake venoms are complex mixtures of protein and peptide components (circa 20–200 per species), commonly referred to as toxins, and this phenotype is underpinned by dozens of gene loci[21]. If borne out, such FP progeny might be at a disadvantage in regards to venom function and incur loss of fitness

Methods

Results

Conclusion