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Sex and age‐biased nematode prevalence in reptiles
Prevalence and intensity of parasitic infections are often higher in male than in female vertebrates. This bias may represent either differences between host sex in exposure or susceptibility to parasites. The former may be due to sex‐specific behaviour of the host, including differential habitat us...
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Published in: | Molecular ecology 2014-08, Vol.23 (15), p.3890-3899 |
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description | Prevalence and intensity of parasitic infections are often higher in male than in female vertebrates. This bias may represent either differences between host sex in exposure or susceptibility to parasites. The former may be due to sex‐specific behaviour of the host, including differential habitat use or diet. Differences in susceptibility are often regarded as a negative effect of male sex steroid hormones on the immune system. Host–parasite dynamics are of great interest in terms of reptile survival, ecology and conservation. We used, for the first time, molecular diagnostics to track nematode parasitism in wild populations of reptiles noninvasively. Using slow worms (Anguis fragilis) as a model species, we investigated the interacting effects of time of year, sex, length, weight and climatic variables on the prevalence of the gastroenterological parasitic nematode Neoxysomatium brevicaudatum. Faeces were collected from three sites over 2 years. There was an interaction between sex and time of year, with lower nematode prevalence in males than in females in July or August (different between years) but a high prevalence in males in April. As the latter is during the slow worm breeding season, this may be the result of testosterone‐induced immunosuppression. A second‐order interaction between slow worm length and weight was found to be significant, with a positive association between prevalence and body condition in young slow worms and a negative association in older slow worms. The convex pattern of nematode prevalence with age that emerged suggests an increase with age‐related exposure and a decrease with age‐related acquired immunity. |
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C</creator><creatorcontrib>Brown, David S ; Symondson, William O. C</creatorcontrib><description>Prevalence and intensity of parasitic infections are often higher in male than in female vertebrates. This bias may represent either differences between host sex in exposure or susceptibility to parasites. The former may be due to sex‐specific behaviour of the host, including differential habitat use or diet. Differences in susceptibility are often regarded as a negative effect of male sex steroid hormones on the immune system. Host–parasite dynamics are of great interest in terms of reptile survival, ecology and conservation. We used, for the first time, molecular diagnostics to track nematode parasitism in wild populations of reptiles noninvasively. Using slow worms (Anguis fragilis) as a model species, we investigated the interacting effects of time of year, sex, length, weight and climatic variables on the prevalence of the gastroenterological parasitic nematode Neoxysomatium brevicaudatum. Faeces were collected from three sites over 2 years. There was an interaction between sex and time of year, with lower nematode prevalence in males than in females in July or August (different between years) but a high prevalence in males in April. As the latter is during the slow worm breeding season, this may be the result of testosterone‐induced immunosuppression. A second‐order interaction between slow worm length and weight was found to be significant, with a positive association between prevalence and body condition in young slow worms and a negative association in older slow worms. The convex pattern of nematode prevalence with age that emerged suggests an increase with age‐related exposure and a decrease with age‐related acquired immunity.</description><identifier>ISSN: 0962-1083</identifier><identifier>EISSN: 1365-294X</identifier><identifier>DOI: 10.1111/mec.12688</identifier><identifier>PMID: 24612272</identifier><language>eng</language><publisher>England: Blackwell Science</publisher><subject>acquired immunity ; adaptive immunity ; Age Factors ; age prevalence ; Anguis fragilis ; Animals ; body condition ; breeding ; breeding season ; Breeding seasons ; Climate change ; Conservation biology ; diagnostic techniques ; diet ; DNA, Helminth - analysis ; feces ; Feces - parasitology ; Female ; females ; Habitat utilization ; habitats ; Hormones ; Host-Parasite Interactions ; Immune system ; immunosuppression ; Lizards - parasitology ; Male ; males ; Nematoda ; Nematoda - isolation & purification ; Nematodes ; Parasites ; Parasitism ; parasitoses ; Reptiles ; Reptiles & amphibians ; Seasons ; Sequence Analysis, DNA ; Sex Factors ; Sexual behavior ; slow worms ; Steroid hormones ; United Kingdom</subject><ispartof>Molecular ecology, 2014-08, Vol.23 (15), p.3890-3899</ispartof><rights>2014 John Wiley & Sons Ltd</rights><rights>2014 John Wiley & Sons Ltd.</rights><rights>Copyright © 2014 John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5538-139cab73364efd10904017db74dc5b4fa3e8ce1135762358219a7dd1caba5c3d3</citedby><cites>FETCH-LOGICAL-c5538-139cab73364efd10904017db74dc5b4fa3e8ce1135762358219a7dd1caba5c3d3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27903,27904</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24612272$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Brown, David S</creatorcontrib><creatorcontrib>Symondson, William O. C</creatorcontrib><title>Sex and age‐biased nematode prevalence in reptiles</title><title>Molecular ecology</title><addtitle>Mol Ecol</addtitle><description>Prevalence and intensity of parasitic infections are often higher in male than in female vertebrates. This bias may represent either differences between host sex in exposure or susceptibility to parasites. The former may be due to sex‐specific behaviour of the host, including differential habitat use or diet. Differences in susceptibility are often regarded as a negative effect of male sex steroid hormones on the immune system. Host–parasite dynamics are of great interest in terms of reptile survival, ecology and conservation. We used, for the first time, molecular diagnostics to track nematode parasitism in wild populations of reptiles noninvasively. Using slow worms (Anguis fragilis) as a model species, we investigated the interacting effects of time of year, sex, length, weight and climatic variables on the prevalence of the gastroenterological parasitic nematode Neoxysomatium brevicaudatum. Faeces were collected from three sites over 2 years. There was an interaction between sex and time of year, with lower nematode prevalence in males than in females in July or August (different between years) but a high prevalence in males in April. As the latter is during the slow worm breeding season, this may be the result of testosterone‐induced immunosuppression. A second‐order interaction between slow worm length and weight was found to be significant, with a positive association between prevalence and body condition in young slow worms and a negative association in older slow worms. The convex pattern of nematode prevalence with age that emerged suggests an increase with age‐related exposure and a decrease with age‐related acquired immunity.</description><subject>acquired immunity</subject><subject>adaptive immunity</subject><subject>Age Factors</subject><subject>age prevalence</subject><subject>Anguis fragilis</subject><subject>Animals</subject><subject>body condition</subject><subject>breeding</subject><subject>breeding season</subject><subject>Breeding seasons</subject><subject>Climate change</subject><subject>Conservation biology</subject><subject>diagnostic techniques</subject><subject>diet</subject><subject>DNA, Helminth - analysis</subject><subject>feces</subject><subject>Feces - parasitology</subject><subject>Female</subject><subject>females</subject><subject>Habitat utilization</subject><subject>habitats</subject><subject>Hormones</subject><subject>Host-Parasite Interactions</subject><subject>Immune system</subject><subject>immunosuppression</subject><subject>Lizards - parasitology</subject><subject>Male</subject><subject>males</subject><subject>Nematoda</subject><subject>Nematoda - isolation & purification</subject><subject>Nematodes</subject><subject>Parasites</subject><subject>Parasitism</subject><subject>parasitoses</subject><subject>Reptiles</subject><subject>Reptiles & amphibians</subject><subject>Seasons</subject><subject>Sequence Analysis, DNA</subject><subject>Sex Factors</subject><subject>Sexual behavior</subject><subject>slow worms</subject><subject>Steroid hormones</subject><subject>United Kingdom</subject><issn>0962-1083</issn><issn>1365-294X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><recordid>eNqF0c9u1DAQBnALgehSOPACEIkLHNJ6PHacHNGqFMQCh7Zib5ZjT6qU_FnsXWhvPALP2CepQ9oekBC--PKbT57PjD0HfgDpHPbkDkAUZfmALQALlYtKrh-yBa8KkQMvcY89ifGCc0Ch1GO2J2QBQmixYPKELjM7-Mye0_Wv33VrI_lsoN5uR0_ZJtAP29HgKGuHLNBm23YUn7JHje0iPbu999nZu6PT5ft89eX4w_LtKndKYZkDVs7WGrGQ1HjgFZcctK-19E7VsrFIpSMAVLoQqEoBldXeQxqyyqHHffZ6zt2E8fuO4tb0bXTUdXagcRcNKCUrpXTa6_9UllChhIm--otejLswpEUmpRFkwWVSb2blwhhjoMZsQtvbcGWAm6l1k1o3f1pP9sVt4q7uyd_Lu5oTOJzBz1Tf1b-TzKej5V1kPk-0cUuX9xM2fDOFRq3M18_H5nS1Fh_XazTTc1_OvrGjseehjebsRHCQ06fLSgDeAHQcodI</recordid><startdate>201408</startdate><enddate>201408</enddate><creator>Brown, David S</creator><creator>Symondson, William O. C</creator><general>Blackwell Science</general><general>Blackwell Publishing Ltd</general><scope>FBQ</scope><scope>BSCLL</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7SN</scope><scope>7SS</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>201408</creationdate><title>Sex and age‐biased nematode prevalence in reptiles</title><author>Brown, David S ; Symondson, William O. C</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5538-139cab73364efd10904017db74dc5b4fa3e8ce1135762358219a7dd1caba5c3d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>acquired immunity</topic><topic>adaptive immunity</topic><topic>Age Factors</topic><topic>age prevalence</topic><topic>Anguis fragilis</topic><topic>Animals</topic><topic>body condition</topic><topic>breeding</topic><topic>breeding season</topic><topic>Breeding seasons</topic><topic>Climate change</topic><topic>Conservation biology</topic><topic>diagnostic techniques</topic><topic>diet</topic><topic>DNA, Helminth - analysis</topic><topic>feces</topic><topic>Feces - parasitology</topic><topic>Female</topic><topic>females</topic><topic>Habitat utilization</topic><topic>habitats</topic><topic>Hormones</topic><topic>Host-Parasite Interactions</topic><topic>Immune system</topic><topic>immunosuppression</topic><topic>Lizards - parasitology</topic><topic>Male</topic><topic>males</topic><topic>Nematoda</topic><topic>Nematoda - isolation & purification</topic><topic>Nematodes</topic><topic>Parasites</topic><topic>Parasitism</topic><topic>parasitoses</topic><topic>Reptiles</topic><topic>Reptiles & amphibians</topic><topic>Seasons</topic><topic>Sequence Analysis, DNA</topic><topic>Sex Factors</topic><topic>Sexual behavior</topic><topic>slow worms</topic><topic>Steroid hormones</topic><topic>United Kingdom</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Brown, David S</creatorcontrib><creatorcontrib>Symondson, William O. C</creatorcontrib><collection>AGRIS</collection><collection>Istex</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Molecular ecology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Brown, David S</au><au>Symondson, William O. C</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Sex and age‐biased nematode prevalence in reptiles</atitle><jtitle>Molecular ecology</jtitle><addtitle>Mol Ecol</addtitle><date>2014-08</date><risdate>2014</risdate><volume>23</volume><issue>15</issue><spage>3890</spage><epage>3899</epage><pages>3890-3899</pages><issn>0962-1083</issn><eissn>1365-294X</eissn><abstract>Prevalence and intensity of parasitic infections are often higher in male than in female vertebrates. This bias may represent either differences between host sex in exposure or susceptibility to parasites. The former may be due to sex‐specific behaviour of the host, including differential habitat use or diet. Differences in susceptibility are often regarded as a negative effect of male sex steroid hormones on the immune system. Host–parasite dynamics are of great interest in terms of reptile survival, ecology and conservation. We used, for the first time, molecular diagnostics to track nematode parasitism in wild populations of reptiles noninvasively. Using slow worms (Anguis fragilis) as a model species, we investigated the interacting effects of time of year, sex, length, weight and climatic variables on the prevalence of the gastroenterological parasitic nematode Neoxysomatium brevicaudatum. Faeces were collected from three sites over 2 years. There was an interaction between sex and time of year, with lower nematode prevalence in males than in females in July or August (different between years) but a high prevalence in males in April. As the latter is during the slow worm breeding season, this may be the result of testosterone‐induced immunosuppression. A second‐order interaction between slow worm length and weight was found to be significant, with a positive association between prevalence and body condition in young slow worms and a negative association in older slow worms. The convex pattern of nematode prevalence with age that emerged suggests an increase with age‐related exposure and a decrease with age‐related acquired immunity.</abstract><cop>England</cop><pub>Blackwell Science</pub><pmid>24612272</pmid><doi>10.1111/mec.12688</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record> |
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subjects | acquired immunity adaptive immunity Age Factors age prevalence Anguis fragilis Animals body condition breeding breeding season Breeding seasons Climate change Conservation biology diagnostic techniques diet DNA, Helminth - analysis feces Feces - parasitology Female females Habitat utilization habitats Hormones Host-Parasite Interactions Immune system immunosuppression Lizards - parasitology Male males Nematoda Nematoda - isolation & purification Nematodes Parasites Parasitism parasitoses Reptiles Reptiles & amphibians Seasons Sequence Analysis, DNA Sex Factors Sexual behavior slow worms Steroid hormones United Kingdom |
title | Sex and age‐biased nematode prevalence in reptiles |
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