THE ORIGIN OF THE SPINNING APPARATUS IN SPIDERS

Abstract

Summary Previous attempts to explain the evolution of spider silk have relied heavily on conjecture. The formulation of testable historical hypotheses to replace such speculation is discussed. The importance of phylogenetic reconstructions and other historical hypotheses for use in generating and testing hypotheses concerning the evolution of specific adaptations is examined. Recent ideas on arachnid phylogeny are reviewed and their relevance to the problem of silk evolution in spiders is explored. Evidence from the analysis of three historical problems (origin of spinnerets, origin of silk glands, original selective pressure favouring evolution of silk) is reviewed from three different frames of reference (in‐group analysis, out‐group analysis, convergence analysis). Several lines of evidence are found which suggest that silk use originated in spiders due to selective pressures associated with reproduction (specifically, the transfer of sperm or the protection of eggs). The prevalence of segmental appendages retained for use in manipulating genital products in both arachnids and non‐arachnid arthropods and the probable placement of spinnerets near the genital opening in ancestral spiders suggest that spinnerets represent modified gonopods. The most primitive types of silk glands are retained in virtually all spiders, in part, for use in the construction of sperm webs and egg sacs. Similar silk glands are found near the genital opening in many male spiders and used in building a portion of the sperm web. The silk of adult arthropods other than spiders is used largely in manipulating or protecting sex cells. If there are multiple functions, use in reproduction is typically one of them. Thus, there is evidence for strong selective pressure favouring the evolution of silk for use in reproduction. Two hypotheses are proposed which are consistent with the conclusion that silk in spiders evolved for reproductive needs (the spermatophore‐sperm web and egg sac hypotheses). Testable predictions of each hypothesis are proposed.