Hydrobiologia

, Volume 808, Issue 1, pp 5–22 | Cite as

Dimorphic male squid show differential gonadal and ejaculate expenditure

  • Lígia H. Apostólico
  • José E. A. R. Marian
CEPHALOPOD ECOLOGY AND LIFE CYCLES

Abstract

Under intense sexual selection, males less successful in fighting and mate guarding often adopt alternative reproductive tactics. In many species, males employing alternative tactics show not only behavioral differences, but also divergences in morphology and physiology, a phenomenon called intrasexual male dimorphism. Herein, we investigated intrasexual male dimorphism in the loliginid squid Doryteuthis plei, associated with alternative mating tactics. We show that small males (sneakers) have spermatophores with discontinuously smaller sperm mass and longer spermatozoa than large males (consorts). Moreover, sneakers produce club-like spermatangia, whereas consorts produce hook-like spermatangia, each type of spermatangia associated with a different female storage site and adoption of a distinct mating position. We also show that dimorphic males have different gonadal investment, sneakers showing higher increment rates in testis mass and higher investment in spermatophoric complex than consorts. Under the complex squid mating system, with two distinct fertilization environments, we hypothesize that sneakers may maximize their reproductive success by both investing more in gonad growth and partitioning ejaculates into extra mating opportunities, whereas consorts may benefit from investment in somatic growth. Squids may be the first example of animals that, even with distinct sperm storage sites, fit the general predictions of sneaks and guards theoretical models.

Keywords

Allocation trade-off Allometry Alternative reproductive tactics Conditional strategy Intrasexual male dimorphism Male–male competition Sperm competition Status dependence 

Notes

Acknowledgements

This study was conducted as part of the first author’s Master dissertation in the Graduate Program in Zoology of the Department of Zoology, at the University of São Paulo (USP). The authors appreciate the financial support and grants provided by CAPES (Coordination for the Improvement of Higher Education Personnel), CAPES/PROEX and CNPq (National Council for Scientific and Technological Development—Proc. 477233/2013-9). The authors are also grateful for the support from the following laboratories and institutions: “Centro de Biologia Marinha” (logistic support for animal collection and maintenance, light microscopy facilities), “Laboratório de Cultivo e Estudos de Cnidaria” (light microscopy facilities), “Laboratório de Entomologia e Aracnologia” (light microscopy facilities), and “Laboratório de Biologia Celular de Invertebrados Marinhos” (citocentrifuge facilities for spermatozoa preparation). The authors specially thank Dr. Alvaro E. Migotto, from “Centro de Biologia Marinha,” for the invaluable assistance during in vitro experimentation and digital filming of the spermatophoric reaction, Dr. Glauco Machado (USP) for his helpful critical reading of the research proposal, Dr. Bruno Buzatto (University of Southwestern Australia) for the inestimable assistance and critical comments concerning statistical analyses, and the colleagues at CIAC 2015 Symposium (Hakodate, Japan) for all comments and suggestions that helped to improve this study. Glauco Machado, Bruno Buzatto, Vlad Laptikhovsky, and an anonymous reviewer helped to improve the quality of the manuscript and are greatly appreciated. This is a contribution of NP-BioMar (Research Center for Marine Biodiversity, USP).

Supplementary material

10750_2017_3145_MOESM1_ESM.pdf (103 kb)
Online Resource 1 Detailed description of the regression model (and equations used), adapted from Eberhard & Gutierrez (1991) original article. This analysis was applied herein for the detection of a body-size switch point (i.e., detection of male intrasexual dimorphism) in the squid Doryteuthis plei. (PDF 104 kb)
10750_2017_3145_MOESM2_ESM.pdf (142 kb)
Online Resource 2 Results of the analysis for detection of male intrasexual dimorphism in Doryteuthis plei, based on the models described in Eberhard & Gutierrez (1991). Regression coefficients and significance tests for each model are provided. For spermatophore length, the best-fit switch point was at 220.2 mm of mantle length (Model 3, adjusted R 2 = 0.891); for sperm mass length, the best-fit switch point was at 215.1 mm of mantle length (Model 3, adjusted R 2 = 0.874); for sperm mass length index (SMLI), the best-fit switch point was at 169.3 mm of mantle length (Model 2, adjusted R 2 = 0.690); and for sperm mass volume, the best-fit switch point was at 205.0 mm of mantle length (Model 2, adjusted R 2 = 0.789). (PDF 142 kb)

Online Resource 3 Digital filming of in vitro experiment of spermatophoric reaction and hook-like spermatangium formation in a consort male (mantle length = 252.0 mm) of the squid Doryteuthis plei, conducted under a Zeiss SV-11 stereomicroscope coupled to a Sony NEX FS700 digital camera. The spermatophore was dissected from the spermatophoric sac of the anesthetized male and placed in a Petri dish filled with filtered seawater. The spermatophoric reaction was induced by rapidly pulling the cap thread, aided by dissecting forceps. The reaction encompasses a series of complex evagination processes of membranes and tunics of the spermatophore, resulting on the formation of a hook-like spermatangium (i.e., everted spermatophore containing the sperm mass). (WMV 26364 kb)

Online Resource 4 Digital filming of in vitro experiment of spermatophoric reaction and club-like spermatangium formation in a sneaker male (mantle length = 106.0 mm) of the squid Doryteuthis plei, conducted under a Zeiss SV-11 stereomicroscope coupled to a Sony NEX FS700 digital camera. The spermatophore was dissected from the spermatophoric sac of the anesthetized male and placed in a Petri dish filled with filtered seawater. The spermatophoric reaction was induced by rapidly pulling the cap thread, aided by dissecting forceps. The reaction encompasses a series of complex evagination processes of membranes and tunics of the spermatophore, resulting on the formation of a club-like spermatangium (i.e., everted spermatophore containing the sperm mass). (WMV 9283 kb)

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Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  • Lígia H. Apostólico
    • 1
  • José E. A. R. Marian
    • 1
  1. 1.Departamento de Zoologia, Instituto de BiociênciasUniversidade de São PauloSão PauloBrazil

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