Sex versus parthenogenesis; immune function in a facultatively parthenogenetic phasmatid (Extatosoma tiaratum)

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Abstract

Facultative parthenogenetic species, in which females can alternate between sex and parthenogenesis, are useful models to investigate the costs and benefits of sex and parthenogenesis, an ongoing issue in biology. The necessary empirical studies comparing the outcomes of alternative reproductive modes on life history traits are rare and focus mainly on traits directly associated with reproductive fitness. Immune function determines the ability of individuals to defend themselves against injury and disease and is therefore likely to have a significant impact on fitness. Here, we used the facultatively parthenogenetic Australian phasmatid, Extatosoma tiaratum, to investigate the effect of both maternal and offspring mode of conception (sexual or parthenogenetic) on offspring immune function (haemocyte concentration, lytic activity and phenoloxidase activity). We show that when parthenogenesis persists beyond one generation, it has negative effects on immune response in terms of haemocyte concentration and lytic activity. Phenoloxidase activity positively correlates with the level of microsatellite heterozygosity. Moreover, immune response decreases across consecutive sampling weeks, suggesting there are physiological constraints with respect to mounting immune responses in close time intervals.

Introduction

Facultative parthenogenesis in which females can reproduce both sexually and parthenogenetically occurs in isolated clades across a broad taxonomic range, including insects, reptiles, fish, birds and sharks (Booth et al., 2012). The adaptive significance of facultative parthenogenesis is poorly understood, but it may provide benefits in environments where the likelihood of sexual reproduction is lower (Stalker, 1956, Gerritsen, 1980). In contrast, sexual reproduction may persist in such species because of the significant fitness costs associated with parthenogenetic reproduction (Stalker, 1956, Carson, 1967, Lamb and Willey, 1979, Hong and Ando, 1998). The necessary empirical studies comparing the outcomes of alternative reproductive modes on life history traits are rare and focus mainly on traits directly associated with reproductive fitness (e.g. Corley and Moore, 1999, Matsuura et al., 2004, Matsuura and Kobayashi, 2007, Sekine and Tojo, 2010). Facultative parthenogenetic species are suitable models to compare costs and benefits of sex and parthenogenesis, an ongoing challenge in biology, because they provide the opportunity to compare directly sexual and parthenogenetic progeny from the same female.

Immune function determines the ability of individuals to defend themselves against injury and disease and is therefore likely to have a significant impact on fitness. Invertebrates lack the highly specific immunological memory typical of the adaptive vertebrate immune system (Pasquier, 2001). However, recent experimental evidence suggests that the innate immune system has memory-like features analogous to adaptive immunity and thus the capacity and degree to which it responds may shift when an animal is exposed to repeated immunological challenges (Kurtz, 2005, Little et al., 2005). Insect immune responses comprise both humoral and cellular components (see Beckage, 2008) and there are three relatively easily derived measures for innate immune responses: 1) haemocyte concentration – a measure of the density of haemocytes within insect haemolymph. These are responsible for the core cellular defence pathways, such as phagocytosis and encapsulation (Ribeiro and Brehélin, 2006); 2) lysozyme-like (lytic) activity – a measures of the capacity of the immune system to lyse bacterial cell walls and thus clear a bacterial infection (Beckage, 2008); and 3) phenoloxidase (PO) activity – which is an important component of the humoral defence pathway, and is involved in the encapsulation response following a foreign challenge such as infection by an endoparasite or cuticular repair (Kanost and Gorman, 2008). It is broadly assumed that these measures provide a realistic indication of the ability of invertebrates to resist disease and infection (Adamo, 2004, Siva-Jothy et al., 2005, Ribeiro and Brehélin, 2006). Direct evidence supporting this assumption includes positive correlations between these immune measures and fitness traits such as survival or offspring production (e.g. Rantala et al., 2002, Siva-Jothy et al., 2005, Lawniczak et al., 2006). Few, if any, studies have investigated empirical relationships between these immune measures and the mode of reproduction.

Here, we used the facultatively parthenogenetic Australian phasmatid, Extatosoma tiaratum, to investigate the trans-generational effect of alternative reproductive modes (sex and parthenogenesis) on immune function. The relative efficacy of immune function in females with sexual and parthenogenetic modes of conception can be compared directly in E. tiaratum. Female E. tiaratum oviposit continuously throughout their adult lives: unfertilized eggs develop into female offspring via parthenogenesis, while fertilised eggs develop into male and female offspring (Carlberg, 1983). The cytological mechanism of parthenogenesis in E. tiaratum (automixis with terminal fusion) results in substantial loss of heterozygosity in the F1 progeny (Alavi et al., 2016), which makes it possible to infer how females, of unknown history, were conceived (sexually or parthenogenetically). We investigated the effect of both maternal and offspring modes of conception on offspring haemocyte concentration, lysozyme-like (lytic) activity and phenoloxidase (PO) activity. In addition, we asked whether immune function varied longitudinally across a five-week sampling period.

Section snippets

Animal maintenance and culturing

A stock population of E. tiaratum was established from eggs and juveniles obtained from the Melbourne Museum (Museums Victoria, Australia). Females were housed in individual cylindrical containers (height: 23 cm; diameter: 25 cm), enclosed by a fine mesh. All insects were provided with ad libitum fresh leaves of various species of Eucalyptus that had been lightly sprayed with water. Eggs were incubated in plastic boxes (16 × 10 × 5 cm) with 5 mm of sand and misted with water weekly. All insect

Determining reproductive history

The microsatellite heterozygosity data revealed that among the F0 females (N = 12), seven (n = 5 allocated to the virgin treatment and n = 2 allocated to the mated treatment) had been conceived sexually and five (all allocated to the mated treatment) had been conceived parthenogenetically (Supplementary Table 1). All F1 females derived from virgin F0 were conceived parthenogenetically (with no heterozygous loci); while three of the mated F0 females also produced parthenogenetic daughters. The

Discussion

This study has two main findings: first, parthenogenesis may have a negative trans-generational effect on at least two components of immune response in E. tiaratum (haemocyte concentration and lytic activity). As the mode of conception of a female is related to her daughter’s ability to up-regulate immune function, this effect is likely a result of the genetic consequences of reproductive modes, rather than the effect of copulation per se (i.e. the effect of seminal fluid components). There was

Acknowledgments

We would like to thank Joanna Durrant for assistance in developing immune protocols, and several referees for their helpful comments. This study was supported by the Holsworth Wildlife Research Endowment and the Albert Shimmins Fund (to YA).

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