Ecological divergence and sexual selection drive sexual size dimorphism in new world pitvipers (Serpentes: Viperidae)

Abstract

Hypotheses for the origin and maintenance of sexual size dimorphism (SSD) fall into three primary categories: (i) sexual selection on male size, (ii) fecundity selection on female size and (iii) ecological selection for genderspecific niche divergence. We investigate the impact of these forces on SSD evolution in New World pitvipers (Crotalinae). We constructed a phylogeny from up to eight genes (seven mitochondrial, one nuclear) for 104 species of NW crotalines. We gathered morphological and ecological data for 82 species for comparative analyses. There is a strong signal of sexual selection on male size driving SSD, but less evidence for fecundity selection on female size across lineages. No support was found for allometric scaling of SSD (Rensch's rule), nor for directional selection for increasing male size (the Fairbairn-Preziosi hypothesis) in NW crotalines. Interestingly, arboreal lineages experience higher rates of SSD evolution and a pronounced shift to female-biased dimorphism. This suggests that fecundity selection on arboreal females exaggerates ecologically mediated dimorphism, whereas sexual selection drives male size in terrestrial lineages. We find that increasing SSD in both directions (male-and female-biased) decreases speciation rates. In NW crotalines, it appears that increasing magnitudes of ecologically mediated SSD reduce rates of speciation, as divergence accumulates within species among sexes, reducing adaptive divergence between populations leading to speciation.

The Deep Origin and Recent Loss of Venom Toxin Genes in Rattlesnakes

“…Based upon the topology of the species tree [22] and the orthology of the C. scutulatus and C. durissus neurotoxins, the most parsimonious inference explaining the distribution of neurotoxic venom is that the most recent common ancestor of this clade possessed the neurotoxin (denoted most recent common ancestor [MRCA] in Figure 2). Thus, the absence of neurotoxins in C. atrox and C. adamanteus would be due to independent lineage-specific gene losses (denoted by Xs in Figure 2).…”

“…It is estimated that an Asian ancestor gave rise to the New World clade ~22 mya [30] and that rattlesnakes evolved ~12–14 mya [22, 30]. In order to better delimit the evolution of the complex and the heterodimeric neurotoxin within pit vipers, we compared the inferred rattlesnake complex with PLA 2 genes that have been characterized from Asian pit vipers.…”

“…We show that the rattlesnake neurotoxin subunit genes arose from a group 2 PLA 2 gene complex that expanded dramatically in the lineage leading to the crotalids and were present in the last common ancestor of rattlesnakes. Remarkably, we find that, despite their relatively recent divergence (4–7 million years ago [mya]) [22], each lineage has deleted three to four entire genes but retains and expresses a different subset of PLA 2 genes. We propose that the rapid evolution of PLA 2 gene number and venom diversity has been catalyzed by non-allelic homologous recombination (NAHR) seeded by conserved blocks of transposon repeats dispersed throughout the complex.…”

Extremely Divergent Haplotypes in Two Toxin Gene Complexes Encode Alternative Venom Types within Rattlesnake Species

“…Viperid venoms are composed of proteins from a limited set of gene families but are distinguished by which family members are expressed and their levels of gene expression. One group, the rattlesnakes (Crotalus and Sistrurus), consists of 36 extant species that radiated over the last 12–14 million years [6, 7]. In general, each rattlesnake species’ venom is one of two main types with distinct protein toxins and modes of subduing prey: a hemorrhagic type as in the North American eastern and western diamondback (C. atrox and C. adamanteus) rattlesnakes or a neurotoxic type as in the South American rattlesnake (C. durissus).…”

The Geography of Morphological Convergence in the Radiations of PacificSebastesRockfishes

“…As the specimens we were able to measure, largely collected by fishing boats or museums, were potentially nonrandom samples with regard to species' typical adult sizes, we substituted log-transformed published maximum TL values (Love et al 2002;Froese and Pauly 2013) as a measure of body size. While maximum sizes are subject to the effects of sampling intensity and extreme observations, in taxa with indeterminate growth and no clear delineation between subadults and adults, maximum size can be a more appropriate measure of adult size than sampled body sizes (e.g., Stephens and Wiens 2009;Hendry et al 2014).…”