Molecular Ecology (2014) 23, 3130–3132
NEWS AND VIEWS
PERSPECTIVE
Why some parasites are widespread and abundant while others are local and rare? M A R C O S R O B A L I N H O L I M A * and S T A F F A N BENSCH† *Programa de Pos-Graduacß~ao em Ci^encias Biologicas, Departamento de Biologia Animal e Vegetal, Universidade Estadual de Londrina, CP 6001, 86051-970, Londrina, Brazil, †Department of Biology, Lund University, Ecology Building, So¨lvegatan 37, 223 62 Lund, Sweden
Abundances and distributions of species are usually associated. This implies that as a species declines in abundance so does the number of sites it occupies. Conversely, when there is an increase in a species’ range size, it is usually followed by an increase in population size (Gaston et al. 2000). This ecological phenomenon, also known as the abundance–occupancy relationship (AOR), is well documented in several species of animals and plants (Gaston et al. 2000) but has been little investigated in parasites. In this issue of Molecular Ecology, Drovetski et al. (2014) investigated the AOR in avian haemosporidians (vector-borne blood parasites) using data from four well-sampled bird communities. In support of the AOR, the research group found that the abundance of parasite cytochrome b lineages (a commonly used proxy for species identification within this group of parasites) was positively linked with the abundance of susceptible avian host species and that the most abundant haemospordian lineages were those with larger ranges. Drovetski et al. (2014) also found evidence for both hypotheses proposed to explain the AOR in parasites: the trade-off hypothesis (TOH) and the niche-breadth hypothesis (NBH). Interestingly, the main predictor of the AOR was the number of susceptible hosts (i.e. number of infected birds) and not the number of host species the parasites were able to exploit. Keywords: Area–occupancy relationship, avian niche-breadth hypothesis, trade-off hypothesis
malaria,
Received 24 April 2014; revised 19 May 2014; accepted 21 May 2014 The TOH stipulates that parasites specializing on single host species need only to adapt to a single immune
Correspondence: Staffan Bensch, Fax: +46-46-2224716; E-mail: staffan. [email protected]
defence system, this in turn would allow them to efficiently replicate and transmit within this host and therefore obtain high prevalence (the proportion of hosts carrying an infection) across the host’s entire range. Conversely, generalist parasites need to circumvent an array of immune systems and may therefore experience reduced replication rates in all of its hosts, reducing both transmission and prevalence. According to the TOH, specialist parasites should be more prevalent (abundant or more frequent) than generalist parasites. Alternatively, the NBH postulates that parasites infecting multiple host species should be more abundant (prevalent) because generalist parasites are capable of colonizing different communities, whereas specialist parasites, confined to a single host species, will be restricted to avian communities with higher abundance of their specific host. Because haemosporidians are transmitted to birds by blood-sucking dipteran vectors, there is a high probability of these parasites being transmitted to suboptimal hosts. Therefore, one may expect from the NBH that the most prevalent avian haemosporidian lineages would be those that exploit a broad range of host species. Evidence for the NBH in avian haemosporidians has already been shown by Hellgren et al. (2009). However, Drovetski et al. (2014) found support for both hypotheses because abundant and widespread haemosporidian lineages (i.e. present in all 4 biogeographical regions studied) included both specialists and generalists (Fig. 1). Clearly, more studies are needed to test the relative importance of the NBH and the TOH. However, the study by Drovetski et al. (2014) proposes that AOR in malaria parasites is strongly driven by the number of susceptible hosts independent of infection strategy. In support for this, the authors found that the most abundant avian host species in their study areas were also the ones disproportionally parasitized. Therefore, if a specialist parasite associates with a species that is abundant and widespread, it will achieve higher abundance and larger range size, the same rationale applies to generalist parasites. If the AOR in malaria parasites is strongly driven by the number of susceptible hosts, it is possible that the range of host species exploited by haemosporidians may depend on the diversity of the bird community. For example, in the Amazon basin, where diversity is high because of the presence of many bird species of small ranges, a generalist host strategy may be better suited than a specialist host strategy. In line with this, a recent study of global haemosporidian diversity found that Plasmodium parasites (typically more of a generalist than Haemoproteus) were highly diverse and prevalent in the Neotropical region (Clark et al. 2014). Conversely, areas of low host diversity with several common species with large ranges may present a
© 2014 John Wiley & Sons Ltd
N E W S A N D V I E W S : P E R S P E C T I V E 3131 (A)
(B)
higher abundance of host specialists. Therefore, both infection strategies may be advantageous depending on host diversity patterns. The high diversity of haemosporidian lineages requires data from thoroughly sampled host communities in order to accurately determine host and geographic range of parasite lineages. Although the study by Drovetski et al. (2014) is based on an impressive data set (2,318 birds of 103 species from four distant communities), less than one-third of the 386 encountered lineages were found in more than one host individual. Moreover, only a small fraction of the lineages (13) were found frequently enough (>30 individual hosts) to be informative when testing the relative importance of the NBH and the TOH. Hence, for the vast majority of lineages (>95%), we do not know the relationship between local abundance, infection strategy and occupancy. Single studies will be unlikely to overcome this problem unless sample sizes are scaled up by orders of magnitude. A way to tackle this problem is to make concerted use of the data collected by different research groups. One such initiative is the MalAvi database (Bensch et al. 2009), an open repository (http://mbio-serv2.mbioekol.lu.se/Malavi/), which presently contains host and geographic data for 1,500 haemosporidian lineages obtained from 850 species of birds. As studies accumulate, MalAvi will eventually provide the data needed to critically test the questions addressed in the study by Drovetski et al. (2014) for a larger number of lineages and along different geographical scales. Most studies of haemosporidian lineages deal with prevalence data, few combine this information with parasitemia (infection intensity), and there is no study we are aware of that has compared parasitemia for the same lineage in different species of wild birds. A prediction from the TOH is that specialists should replicate more efficiently (higher parasitemia) in their host than generalists (on average) © 2014 John Wiley & Sons Ltd
Fig. 1 Parus major captured in Morocco infected with SGS1, a generalist lineage within the species Plasmodium relictum (A); and Fringilla coelebs captured in Morocco infected with CCF2 a specialist lineage of Haemoproteus sp. that has not yet been morphologically described (B). Both lineages were present in the four geographical regions studied by Drovetski et al. (2014). Pictures of birds were kindly provided by Sergei V. Drovetski, while Vanessa A. Mata provided the blood smear pictures.
across their set of hosts. Parasitemia can be accurately estimated both by microscopic examination of blood smears and using qPCR (Zehtindjiev et al. 2008), although the low chronic infection levels that typically prevail in wild populations are difficult to estimate accurately. It has recently been shown that the chronic stage of infection is positively correlated with parasitemia during the acute phase of infection in great reed warblers experimentally infected with Plasmodium ashfordi (Asghar et al. 2012). Moreover, in wild birds of the same species, the individual level of chronic parasitemia is significantly correlated across years (Asghar et al. 2011). Together, these two findings suggest that estimates of chronic level parasitemia can be measured accurately and that it carries information about the more important acute phase of infection that is brief and difficult to study in wild birds; however, it remains to be tested whether these findings apply to other species and whether chronic parasitemia also differs between species. It is also important to establish whether a bird species is indeed a competent host for the haemosporidian lineage (Valki unas et al. 2009). It has recently been found that parasites infecting noncompetent hosts sometimes replicate in exo-erythrocytic tissues without forming gametocytes (the transmission stages of the parasite) in the blood (Olias et al. 2011). DNA from these exo-erythrocytic replication places can spill over into the blood and be detected by PCR. Future studies will be more accurate in assessing host range if blood smears are analysed in parallel with PCR to establish the presence of gametocytes. There are two research gaps that need further development in order to understand the AOR. One is the role of vectors in shaping the diversity and distribution of haemosporidians (Santiago-Alarcon et al. 2012). For example, should we expect generalist lineages such as SGS1 to be transmitted by several different vector species? Should we expect to find an AOR when we look at the vector-avian
3132 N E W S A N D V I E W S : P E R S P E C T I V E haemosporidian part of the equation? The other research gap is the development of molecular markers targeting independent multiple loci, for example, microsatellites or orthologs to merozoite surface protein genes commonly used for population genetic studies of mammalian malaria parasites. Development of these markers will allow researchers to identify the true host breadth of parasites. For example, the lineage SGS1 – a member of the morphospecies Plasmodium relictum – has been recorded in 83 hosts species. But how confident can we be that this lineage represents the same species in all its hosts without examining population genetic data? In conclusion, avian haemosporidians offer a rich model system to address a broad set of questions in ecology and evolution. We encourage future studies to employ both microscopy and PCR, to utilize the MalAvi database and to direct resources towards studies of vectors’ role in transmission patterns, the least known component in this parasitevector-host system. We also recommend researchers to have a research focus based on vector and bird communities instead of single species studies, because the former is more likely to elucidate general ecological and evolutionary patterns.
References Asghar M, Hasselquist D, Bensch S (2011) Are chronic avian haemosporidian infections costly in wild birds? Journal of Avian Biology, 42, 530–537. Asghar M, Westerdahl H, Zehtindjiev P et al. (2012) Primary peak and chronic malaria infection levels are correlated in experimentally infected great reed warblers. Parasitology, 139, 1246–1252.
Bensch S, Hellgren O, Perez-Tris J (2009) MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Molecular Ecology Resources, 9, 1353–1358. Clark NJ, Clegg SM, Lima MR (2014) A review of global diversity in avian haemosporidians (Plasmodium and Haemoproteus: Haemosporida): new insights from molecular data. International Journal for Parasitology, 44, 329–338. Drovetski SV, Aghayan SA, Mata VA et al. (2014) Does the nichebreath or trade-off hypothesis explain the abundance-occupancy relationship in avian haemosporidia. Molecular Ecology, 23, 3322– 3329. Gaston KJ, Blackburn TM, Greenwood JJ et al. (2000) Abundance– occupancy relationships. Journal of Applied Ecology, 37, 39–59. Hellgren O, Perez-Tris J, Bensch S (2009) A jack-of-all-trades and still a master of some: prevalence and host range in avian malaria and related blood parasites. Ecology, 90, 2840–2849. Olias P, Weglin M, Zenker W et al. (2011) Avian malaria deaths in parrots, Europe. Emerging Infectious Diseases, 17, 950–952. Santiago-Alarcon D, Palinauskas V, Schaefer HM (2012) Diptera vectors of avian Haemosporidian parasites: untangling parasite life cycles and their taxonomy. Biological Reviews, 87, 928–964. Valki unas G, Iezhova TA, Loiseau C, Sehgal RNM (2009) Nested cytochrome b polymerase chain reaction diagnostics detect sporozoites of hemosporidian parasites in peripheral blood of naturally infected birds. Journal of Parasitology, 95, 1512–1515. Zehtindjiev P, Ilieva M, Westerdahl H et al. (2008) Dynamics of parasitemia of malaria parasites in a naturally and experimentally infected migratory songbird, the great reed warbler Acrocephalus arundinaceus. Experimental Parasitology, 119, 99–110.
M.R.L. and S.B. wrote the paper together. doi: 10.1111/mec.12809
© 2014 John Wiley & Sons Ltd
NEWS AND VIEWS
PERSPECTIVE
Why some parasites are widespread and abundant while others are local and rare? M A R C O S R O B A L I N H O L I M A * and S T A F F A N BENSCH† *Programa de Pos-Graduacß~ao em Ci^encias Biologicas, Departamento de Biologia Animal e Vegetal, Universidade Estadual de Londrina, CP 6001, 86051-970, Londrina, Brazil, †Department of Biology, Lund University, Ecology Building, So¨lvegatan 37, 223 62 Lund, Sweden
Abundances and distributions of species are usually associated. This implies that as a species declines in abundance so does the number of sites it occupies. Conversely, when there is an increase in a species’ range size, it is usually followed by an increase in population size (Gaston et al. 2000). This ecological phenomenon, also known as the abundance–occupancy relationship (AOR), is well documented in several species of animals and plants (Gaston et al. 2000) but has been little investigated in parasites. In this issue of Molecular Ecology, Drovetski et al. (2014) investigated the AOR in avian haemosporidians (vector-borne blood parasites) using data from four well-sampled bird communities. In support of the AOR, the research group found that the abundance of parasite cytochrome b lineages (a commonly used proxy for species identification within this group of parasites) was positively linked with the abundance of susceptible avian host species and that the most abundant haemospordian lineages were those with larger ranges. Drovetski et al. (2014) also found evidence for both hypotheses proposed to explain the AOR in parasites: the trade-off hypothesis (TOH) and the niche-breadth hypothesis (NBH). Interestingly, the main predictor of the AOR was the number of susceptible hosts (i.e. number of infected birds) and not the number of host species the parasites were able to exploit. Keywords: Area–occupancy relationship, avian niche-breadth hypothesis, trade-off hypothesis
malaria,
Received 24 April 2014; revised 19 May 2014; accepted 21 May 2014 The TOH stipulates that parasites specializing on single host species need only to adapt to a single immune
Correspondence: Staffan Bensch, Fax: +46-46-2224716; E-mail: staffan. [email protected]
defence system, this in turn would allow them to efficiently replicate and transmit within this host and therefore obtain high prevalence (the proportion of hosts carrying an infection) across the host’s entire range. Conversely, generalist parasites need to circumvent an array of immune systems and may therefore experience reduced replication rates in all of its hosts, reducing both transmission and prevalence. According to the TOH, specialist parasites should be more prevalent (abundant or more frequent) than generalist parasites. Alternatively, the NBH postulates that parasites infecting multiple host species should be more abundant (prevalent) because generalist parasites are capable of colonizing different communities, whereas specialist parasites, confined to a single host species, will be restricted to avian communities with higher abundance of their specific host. Because haemosporidians are transmitted to birds by blood-sucking dipteran vectors, there is a high probability of these parasites being transmitted to suboptimal hosts. Therefore, one may expect from the NBH that the most prevalent avian haemosporidian lineages would be those that exploit a broad range of host species. Evidence for the NBH in avian haemosporidians has already been shown by Hellgren et al. (2009). However, Drovetski et al. (2014) found support for both hypotheses because abundant and widespread haemosporidian lineages (i.e. present in all 4 biogeographical regions studied) included both specialists and generalists (Fig. 1). Clearly, more studies are needed to test the relative importance of the NBH and the TOH. However, the study by Drovetski et al. (2014) proposes that AOR in malaria parasites is strongly driven by the number of susceptible hosts independent of infection strategy. In support for this, the authors found that the most abundant avian host species in their study areas were also the ones disproportionally parasitized. Therefore, if a specialist parasite associates with a species that is abundant and widespread, it will achieve higher abundance and larger range size, the same rationale applies to generalist parasites. If the AOR in malaria parasites is strongly driven by the number of susceptible hosts, it is possible that the range of host species exploited by haemosporidians may depend on the diversity of the bird community. For example, in the Amazon basin, where diversity is high because of the presence of many bird species of small ranges, a generalist host strategy may be better suited than a specialist host strategy. In line with this, a recent study of global haemosporidian diversity found that Plasmodium parasites (typically more of a generalist than Haemoproteus) were highly diverse and prevalent in the Neotropical region (Clark et al. 2014). Conversely, areas of low host diversity with several common species with large ranges may present a
© 2014 John Wiley & Sons Ltd
N E W S A N D V I E W S : P E R S P E C T I V E 3131 (A)
(B)
higher abundance of host specialists. Therefore, both infection strategies may be advantageous depending on host diversity patterns. The high diversity of haemosporidian lineages requires data from thoroughly sampled host communities in order to accurately determine host and geographic range of parasite lineages. Although the study by Drovetski et al. (2014) is based on an impressive data set (2,318 birds of 103 species from four distant communities), less than one-third of the 386 encountered lineages were found in more than one host individual. Moreover, only a small fraction of the lineages (13) were found frequently enough (>30 individual hosts) to be informative when testing the relative importance of the NBH and the TOH. Hence, for the vast majority of lineages (>95%), we do not know the relationship between local abundance, infection strategy and occupancy. Single studies will be unlikely to overcome this problem unless sample sizes are scaled up by orders of magnitude. A way to tackle this problem is to make concerted use of the data collected by different research groups. One such initiative is the MalAvi database (Bensch et al. 2009), an open repository (http://mbio-serv2.mbioekol.lu.se/Malavi/), which presently contains host and geographic data for 1,500 haemosporidian lineages obtained from 850 species of birds. As studies accumulate, MalAvi will eventually provide the data needed to critically test the questions addressed in the study by Drovetski et al. (2014) for a larger number of lineages and along different geographical scales. Most studies of haemosporidian lineages deal with prevalence data, few combine this information with parasitemia (infection intensity), and there is no study we are aware of that has compared parasitemia for the same lineage in different species of wild birds. A prediction from the TOH is that specialists should replicate more efficiently (higher parasitemia) in their host than generalists (on average) © 2014 John Wiley & Sons Ltd
Fig. 1 Parus major captured in Morocco infected with SGS1, a generalist lineage within the species Plasmodium relictum (A); and Fringilla coelebs captured in Morocco infected with CCF2 a specialist lineage of Haemoproteus sp. that has not yet been morphologically described (B). Both lineages were present in the four geographical regions studied by Drovetski et al. (2014). Pictures of birds were kindly provided by Sergei V. Drovetski, while Vanessa A. Mata provided the blood smear pictures.
across their set of hosts. Parasitemia can be accurately estimated both by microscopic examination of blood smears and using qPCR (Zehtindjiev et al. 2008), although the low chronic infection levels that typically prevail in wild populations are difficult to estimate accurately. It has recently been shown that the chronic stage of infection is positively correlated with parasitemia during the acute phase of infection in great reed warblers experimentally infected with Plasmodium ashfordi (Asghar et al. 2012). Moreover, in wild birds of the same species, the individual level of chronic parasitemia is significantly correlated across years (Asghar et al. 2011). Together, these two findings suggest that estimates of chronic level parasitemia can be measured accurately and that it carries information about the more important acute phase of infection that is brief and difficult to study in wild birds; however, it remains to be tested whether these findings apply to other species and whether chronic parasitemia also differs between species. It is also important to establish whether a bird species is indeed a competent host for the haemosporidian lineage (Valki unas et al. 2009). It has recently been found that parasites infecting noncompetent hosts sometimes replicate in exo-erythrocytic tissues without forming gametocytes (the transmission stages of the parasite) in the blood (Olias et al. 2011). DNA from these exo-erythrocytic replication places can spill over into the blood and be detected by PCR. Future studies will be more accurate in assessing host range if blood smears are analysed in parallel with PCR to establish the presence of gametocytes. There are two research gaps that need further development in order to understand the AOR. One is the role of vectors in shaping the diversity and distribution of haemosporidians (Santiago-Alarcon et al. 2012). For example, should we expect generalist lineages such as SGS1 to be transmitted by several different vector species? Should we expect to find an AOR when we look at the vector-avian
3132 N E W S A N D V I E W S : P E R S P E C T I V E haemosporidian part of the equation? The other research gap is the development of molecular markers targeting independent multiple loci, for example, microsatellites or orthologs to merozoite surface protein genes commonly used for population genetic studies of mammalian malaria parasites. Development of these markers will allow researchers to identify the true host breadth of parasites. For example, the lineage SGS1 – a member of the morphospecies Plasmodium relictum – has been recorded in 83 hosts species. But how confident can we be that this lineage represents the same species in all its hosts without examining population genetic data? In conclusion, avian haemosporidians offer a rich model system to address a broad set of questions in ecology and evolution. We encourage future studies to employ both microscopy and PCR, to utilize the MalAvi database and to direct resources towards studies of vectors’ role in transmission patterns, the least known component in this parasitevector-host system. We also recommend researchers to have a research focus based on vector and bird communities instead of single species studies, because the former is more likely to elucidate general ecological and evolutionary patterns.
References Asghar M, Hasselquist D, Bensch S (2011) Are chronic avian haemosporidian infections costly in wild birds? Journal of Avian Biology, 42, 530–537. Asghar M, Westerdahl H, Zehtindjiev P et al. (2012) Primary peak and chronic malaria infection levels are correlated in experimentally infected great reed warblers. Parasitology, 139, 1246–1252.
Bensch S, Hellgren O, Perez-Tris J (2009) MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Molecular Ecology Resources, 9, 1353–1358. Clark NJ, Clegg SM, Lima MR (2014) A review of global diversity in avian haemosporidians (Plasmodium and Haemoproteus: Haemosporida): new insights from molecular data. International Journal for Parasitology, 44, 329–338. Drovetski SV, Aghayan SA, Mata VA et al. (2014) Does the nichebreath or trade-off hypothesis explain the abundance-occupancy relationship in avian haemosporidia. Molecular Ecology, 23, 3322– 3329. Gaston KJ, Blackburn TM, Greenwood JJ et al. (2000) Abundance– occupancy relationships. Journal of Applied Ecology, 37, 39–59. Hellgren O, Perez-Tris J, Bensch S (2009) A jack-of-all-trades and still a master of some: prevalence and host range in avian malaria and related blood parasites. Ecology, 90, 2840–2849. Olias P, Weglin M, Zenker W et al. (2011) Avian malaria deaths in parrots, Europe. Emerging Infectious Diseases, 17, 950–952. Santiago-Alarcon D, Palinauskas V, Schaefer HM (2012) Diptera vectors of avian Haemosporidian parasites: untangling parasite life cycles and their taxonomy. Biological Reviews, 87, 928–964. Valki unas G, Iezhova TA, Loiseau C, Sehgal RNM (2009) Nested cytochrome b polymerase chain reaction diagnostics detect sporozoites of hemosporidian parasites in peripheral blood of naturally infected birds. Journal of Parasitology, 95, 1512–1515. Zehtindjiev P, Ilieva M, Westerdahl H et al. (2008) Dynamics of parasitemia of malaria parasites in a naturally and experimentally infected migratory songbird, the great reed warbler Acrocephalus arundinaceus. Experimental Parasitology, 119, 99–110.
M.R.L. and S.B. wrote the paper together. doi: 10.1111/mec.12809
© 2014 John Wiley & Sons Ltd
