A Widespread and Distinctive Form of Amphipod Intersexuality Not Induced by Known Feminising Parasites

Short, Stephen; Yang, Guanghui; Kille, Peter; Ford, Alex T.

doi:10.1159/000343779

Cited by 15 publications

(25 citation statements)

References 31 publications

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“…haemobaphes were much like those previously reported in Polish waters (Bacela, Konopacka & Grabowski, 2009). To our knowledge, this is the highest prevalence of male intersexuality recorded in an amphipod population (McCurdy et al, 2004;Ford & Fernandes, 2005;Short et al, 2012b;Yang et al, 2011) and is the first evidence clearly linking D. berillonum with amphipod intersexuality (Terry et al, 2004;Yang et al, 2011). Other Dictyocoela species have been linked to both abnormal sexual phenotypes and female-biased sex ratios (Terry et al, 2004;Short et al, 2012a), however, the lack of female-bias in D. haemobaphes suggests D. berillonum is unable to fully convert males in to females.…”

Section: Discussionsupporting

confidence: 84%

Pronounced and prevalent intersexuality does not impede the ‘Demon Shrimp’ invasion

Etxabe

Short

Flood

et al. 2015

Preprint

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Crustacean intersexuality is widespread and often linked to infection by sex-distorting parasites. However, unlike vertebrate intersexuality, its association with sexual dysfunction is unclear and remains a matter of debate. The 'Demon Shrimp', Dikerogammarus haemobaphes, an amphipod that has invaded continental waterways, has recently become widespread in Britain. Intersexuality has been noted in D.haemobaphes but not investigated further. We hypothesise that a successful invasive population should not display a high prevalence of intersexuality if this condition represents a truly dysfunctional phenotype. In addition, experiments have indicated that particular parasite burdens in amphipods may facilitate invasions. The rapid and ongoing invasion of British waterways represents an opportunity to determine whether these hypotheses are consistent with field observations. This study investigates the parasites and sexual phenotypes of D. haemobaphes in British waterways, characterising parasite burdens using molecular screening, and make comparisons with the threatened Gammarus pulex natives. We reveal that invasive and native populations have distinct parasitic profiles, suggesting the loss of G. pulex may have parasite-mediated eco-system impacts. Furthermore, the parasite burdens are consistent with those previously proposed to facilitate biological invasions. Our study also indicates that while no intersexuality occurs in the native G. pulex, approximately 50% of D. haemobaphes males present pronounced intersexuality associated with infection by the microsporidian Dictyocoela berillonum. This unambiguously successful invasive population presents, to our knowledge, the highest reported prevalence of male intersexuality. This is the clearest evidence to date that such intersexuality does not represent a form of debilitating sexual dysfunction that negatively impacts amphipod populations.PeerJ reviewing PDF | (v2014:11:3025:1:0:NEW 9 Jan 2015) PrePrints 90 stubs, sputter coated with gold-palladium and examined using a scanning electron microscope (JEOL 91 6060LV) operating in high vacuum mode with a secondary electron detector active at an acceleration 92 voltage of 10kV. Images were cropped and colourised using Adobe Photoshop (CS5v12). 94 PCR screen95 DNA was purified from internal animal tissue (excluding gut) or eggs using the DNeasy Blood and 96 Tissue Kit (Qiagen, UK). Samples were screened using previously described PCR primers for general 97 parasites (Table 1). PCR reactions were performed in 25 l volumes containing 10 ng of DNA as 98 template, 1 U of Taq polymerase (Promega, UK), 5 l of 5x PCR buffer, 1.25 mM MgCl 2 and 0.4 mM of 99 each corresponding primer. Quality of the DNA samples were analysed using the primers 1073F and 100 18SR (Table 1) which amplified a 867bp product of the host 18S. 102 103 Sequence identification104 PCR products were analysed using agarose gel electrophoresis containing 1x GelGreen TM (Cambridge 105 Bioscience, UK) for the presence of bands potentially representing amplifi...

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Section: Discussionsupporting

confidence: 84%

Pronounced and prevalent intersexuality does not impede the ‘Demon Shrimp’ invasion

Etxabe

Short

Flood

et al. 2015

Preprint

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“…Intersexuality and the associated reproductive costs can occur in amphipods of both sexes (Ford et al, 2003;Ford et al, 2004b;Yang et al, 2008). In addition, it is known that E. marinus males present two morphologically and transcriptomically distinct intersex phenotypes, termed external and internal intersexuality (Ford et al, 2005a;Yang et al, 2008;Short et al, 2012a). External intersex males possess rudimental brood plates (oostegites), a feature normally associated with females, and sometimes exhibit an ovotestis (consisting of a pronounced oviduct-like structure on the testes as described in Ford et al, 2005b).…”

Section: Introductionmentioning

confidence: 99%

Vitellogenin is not an appropriate biomarker of feminisation in a Crustacean

Short¹,

Yang²,

Kille³

et al. 2014

Aquatic Toxicology

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The expression of the yolk protein vitellogenin (Vtg) has been used as a biomarker of feminisation in multiple fish species throughout the world. Since the late 1990s, researchers have attempted to develop similar biomarkers to address whether reproductive endocrine disruption also occurs in the males of invertebrate groups such as the Crustacea. To date, the vast majority of studies investigating Vtg induction in male Crustacea have resulted in negative or inconclusive results, leading researchers to question the utility of Vtg expression as a biomarker in this taxon. This study measured the expression of Vtg genes in two intersex phenotypes (termed internal and external) found in the male amphipod, Echinogammarus marinus, and compared them with those of normal males and females. Males presenting the external intersex phenotype are infected with known feminising parasites and display a variety of feminised traits including oviduct structures on their testes and external female brood plates (oostegites). The internal intersex male phenotype, that displays a pronounced oviduct structure on the testes without the external intersex characteristics, is not parasite infected and it is thought to be a result of environmental contamination. Given their morphology, these phenotypes might be considered highly 'feminised' or 'de-masculinised' and can be utilised to test the suitability of feminisation biomarkers. The E. marinus transcriptome was searched for genes resembling Vtg and two sequences were revealed, that we subsequently refer to as Vtg1 and Vtg2. Results from a high-throughput transcriptomic sequencing screen of gonadal cDNA libraries suggested that very low expression (in this manuscript gene transcription is taken to represent gene expression, although it is acknowledged that in addition to transcription, translation, transcript processing, mRNA stability and protein stability can regulate gene expression) of Vtg1 and Vtg2 in normal males (ESTs=1 and 0 for Vtg1 and Vtg2, respectively), internal intersex males (ESTs=0 for both Vtg sequences) and external intersex males (ESTs=5 and 0 for Vtg1 and Vtg2, respectively). In contrast, the sequencing suggested notable levels of expression of both Vtg genes in females (ESTs=1133 and 84 for Vtg1 and Vtg2, respectively). Subsequent qPCR analysis validates these expression levels, with the signal for Vtg1 and Vtg2 transcripts in all male phenotypes being indistinguishable from that caused by contamination of trace levels of genomic DNA or the low-level amplification non-target sequences. These findings suggest that Vtg expression is not notably induced in highly feminised amphipods and is therefore not an appropriate biomarker of feminisation/de-masculination in crustaceans. We discuss our findings in the context of previous attempts to measure Vtg in male crustaceans and suggest a requirement for more appropriate taxon-specific biomarkers to monitor feminisation in these groups.

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“…To date, several studies have investigated the effect of EDs on amphipods (reviewed by Kunz et al 2010, Grilo & Rosa 2017, but additional infection with microsporidians as a confounding factor was only rarely considered (Ford et al 2006, Gismondi et al 2017. Accordingly, it is generally accepted that the phenomenon of intersex in crustaceans can be induced by various factors, including chemicals and parasites, but the proximate cause for intersex individuals is often not clear (Ford et al 2004, Ford & Fernandes 2005, Hyne 2011, Ford 2012, Short et al 2012a.…”

Section: Microsporidiamentioning

confidence: 99%

Amphipod parasites may bias results of ecotoxicological research

Grabner¹,

Sures²

2019

Dis. Aquat. Org.

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Amphipods are commonly used test organisms in ecotoxicological studies. Nevertheless, their naturally occurring parasites have mostly been neglected in these investigations, even though several groups of parasites can have a multitude of effects, e.g. on host survival, physiology, or behavior. In the present review, we summarize the knowledge on the effects of Microsporidia and Acanthocephala, 2 common and abundant groups of parasites in amphipods, on the outcome of ecotoxicological studies. Parasites can have significant effects on toxicological endpoints (e.g. mortality, biochemical markers) that are unexpected in some cases (e.g. down-regulation of heat shock protein 70 response in infected individuals). Therefore, parasites can bias the interpretation of results, for example if populations with different parasite profiles are compared, or if toxicological effects are masked by parasite effects. With the present review, we would like to encourage ecotoxicologists to consider parasites as an additional factor if field-collected test organisms are analyzed for biomarkers. Additionally, we suggest intensification of research activities on the effects of parasites in amphipods in connection with other stressors to disentangle parasite and pollution effects and to improve our understanding of parasite effects in this host taxon.

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A Widespread and Distinctive Form of Amphipod Intersexuality Not Induced by Known Feminising Parasites

Cited by 15 publications

References 31 publications

Pronounced and prevalent intersexuality does not impede the ‘Demon Shrimp’ invasion

Pronounced and prevalent intersexuality does not impede the ‘Demon Shrimp’ invasion

Vitellogenin is not an appropriate biomarker of feminisation in a Crustacean

Amphipod parasites may bias results of ecotoxicological research

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