A Dwarf Male Reversal in Bone-Eating Worms

Abstract

Darwin hypothesized that sexes in a species should be similar unless sexual selection, fecundity selection, or resource partitioning has driven them apart. Male dwarfism has evolved multiple times in a range of animals, raising questions about factors that drive such extreme size dimorphism. Ghiselin noted that dwarf males are more common among smaller marine animals, and especially among sedentary and sessile species living at low densities, where mates are difficult to find, or in deep-sea environments with limited energy sources. These benefits of male dwarfism apply well to Osedax (Annelida: Siboglinidae), bone-eating marine worms. Osedax males, notable for extreme sexual size dimorphism (SSD), are developmentally arrested larvae that produce sperm from yolk reserves. Harems of dwarf males reside in the lumen of the tube surrounding a female. Herein, we describe Osedax priapus n. sp., a species that deviates remarkably by producing males that anchor into, and feed on, bone via symbiont-containing "roots," just like female Osedax. Phylogenetic analyses revealed O. priapus n. sp. as a derived species, and the absence of dwarf males represents a character reversal for this genus. Some dwarf male features are retained due to functional and morphological constraints. Since O. priapus n. sp. males are anchored in bone, they possess an extensible trunk that allows them to roam across the bone to contact and inseminate females. Evolutionary and ecological implications of a loss of male dwarfism are discussed.

An inordinate fondness for Osedax (Siboglinidae: Annelida): Fourteen new species of bone worms from California

“…Missing values indicate BS < 50% and PP < 0.7. Six major Osedax clades are distinguished, following Vrijenhoek et al (2009), Rouse et al (2015) and Taboada et al (2015). The various forms of palps (or absence thereof in the case of O. jabba n.…”

“…Figure 4D Osedax 'nude-palp-B' Rouse et al 2011;Rouse et al 2009;Rouse et al 2015;Vrijenhoek et al 2009) Material examined. Holotype: SIO-BIC A1643 palps only (GenBank COI sequence EU235218), fixed in formalin preserved in ethanol, collected from cow bones deployed at 2898 meters depth in Monterey Submarine Canyon, California (36°36.606'N; 122°26.122'W) ROV Tiburon dive number 1069, Oct. 1, 2007.…”

“…Fig. 8 'nude-palp-G', 'nude palp #20' (Higgs et al 2014;Rouse et al 2015) Material examined. Diagnosis and description.…”

“…Figure 16 'orange collar' (Braby et al 2007;Rouse et al 2009;Rouse et al 2015;Tresguerres et al 2013;Vrijenhoek et al 2009) 'sp.4 SBJ-2006' (GenBank COI sequence DQ996639, DQ996641-2) FIGURE 16. Osedax packardorum n.…”

“…Bones from naturally occurring and experimentally-deployed cetacean, pinniped, bovid, and teleost bones were deployed and collected by remotely operated vehicle (ROV) over the course of 15 years (details available in Braby et al 2007;Jones et al 2008;Rouse et al 2011;Rouse et al 2015;Vrijenhoek et al 2009). Additional bone samples of turkey (Meleagris gallopavo) and green turtle bones (Chelonia mydas), not reported in previous studies, were deployed at 1018 m depth on 10/29/2010 and 5/25/2010, respectively and recovered on 6/2/2011.…”