The evolutionary implications of conflict between parasites with different transmission modes

Edward Owen Jones, Andrew White, Michael Boots

Research output: Contribution to journalArticle

14 Citations (Scopus)

Abstract

Understanding the processes that shape the evolution of parasites is a key challenge for evolutionary biology. It is well understood that different parasites may often infect the same host and that this may have important implications to the evolutionary behavior. Here we examine the evolutionary implications of the conflict that arises when two parasite species, one vertically transmitted and the other horizontally transmitted, infect the same host. We show that the presence of a vertically transmitted parasite (VTP) often leads to the evolution of higher virulence in horizontally transmitted parasites (HTPs), particularly if the VTPs are feminizing. The high virulence in some HTPs may therefore result from coinfection with cryptic VTPs. The impact of an HTP on a VTP evolution depends crucially on the nature of the life-history trade-offs. Fast virulent HTPs select for intermediate feminization and virulence in VTPs. Coevolutionary models show similar insights, but emphasize the importance of host life span to the outcome, with higher virulence in both types of parasite in short-lived hosts. Overall, our models emphasize the interplay of host and parasite characteristics in the evolutionary outcome and point the way for further empirical study.

Host parasite theory often considers the impact of a single parasite on the dynamics of a single host. However, in natural systems hosts are often challenged by multiple parasites (Woolhouse et al. 2000; Haine et al. 2005; Woolhouse and Gowtage-Sequeria 2005) and this is of course likely to have important implications to the evolutionary dynamics of both parasites and hosts. For example, superinfection, where an invading strain displaces a resident strain in an individual host, often selects for more virulent and competitive parasites (Levin and Pimental 1981; Bremermann and Pickering 1983; Nowak and May 1994). If parasites coinfect the same individual, both within host and population level interactions become important, there are a range of outcomes resulting from multiple infections (Nowak and May 1994; van Baalen and Sabelis 1995; Brown et al. 2002) and in certain circumstances lead to the evolution of greater virulence and the possibility of parasite coexistence (Mosquera and Adler 1998). When parasites that share the same host have different transmission modes and in particular when there is vertically transmission from parent to offspring, conflicts arise. VTPs and horizontally transmitted parasites (HTPs) are both selected to minimize the additional mortality that infection causes. Reduced virulence benefits vertically transmitted parasites (VTPs) by extending the period of host reproduction from infected individuals and equally benefits HTPs by lengthening the infectious period. However, while the birth rate of the infected host is vital for the persistence and spread of a VTP, the fitness of HTPs is not directly affected by a change in host birth rate. Indeed, HTPs will be selected to castrate hosts if this leads to increased transmission (Jaenike 1996; O’Keefe and Antonovics 2002). Here, we examine, theoretically, the evolutionary implications of the resulting conflict over host reproduction between parasites with different transmission modes.

Vertically transmitted parasites are particularly common in invertebrates (Werren 1997; Hogg et al. 2002; Kelly et al. 2003; Stouthamer et al. 2009) but are found across many taxa (Mims 1981). However, purely VTPs that cause virulence to their host will not persist without some other mechanism that compensates for this virulence (Fine 1975; Lipsitch et al. 1995). An important mechanism, by which a virulent VTP may persist, is the manipulation of the host's reproductive output through altering the sex ratio of the host by either increasing the total number of females born, converting males to females (feminization) or by male killing (Werren 1997; Kageyama et al. 2002; Cordaux et al. 2004; Zeh and Zeh 2006). Hurst (1993) showed, using theory that a sex-ratio distorting purely VTP can be maintained in a population even when there is selection against infected hosts by increasing the number of females born in each cohort. There is also evidence that some VTPs may protect the host against other natural enemies (Oliver et al. 2003; Haine et al. 2005). Recently, theory (Lively et al. 2005; Faeth et al. 2007; Jones et al. 2007) has shown that a purely VTP that causes some virulence to the host is able to persist by protecting the host from a virulent HTP. Furthermore, the greater the virulence of the HTP the easier for the vertical host to persist (Jones et al. 2007). Parasites that transmit vertically may also persist if they transmit to some extent horizontally (Busenburg et al. 1983; Regniere 1984) and in nature many pathogens may indeed possess both means of transmission (Burden et al. 2002; Hackett et al. 2005; Zhou et al. 2005). The evolutionary dynamics of parasites that possess both vertical and horizontal transmission modes have been examined in detail by Lipsitch et al. (1996). A key result is that as parasite numbers increase, they select for greater vertical transmission, due to both the higher potential for generation-to-generation infection and reduced encounters with susceptible individuals (Lipsitch et al. 1996). However, the evolutionary dynamics of purely HTPs and purely VTPs that coinfect the same hosts have not been considered in detail.

Here, our aim is to understand the evolutionary behavior of parasite pathogenicity arising from conflict between two different parasite species that can both infect the same host. We consider a purely VTP, maintained in populations through the manipulation of host reproduction, and assume that it coinfects with an HTP. We start with evolutionary models that examine how in turn the presence of a VTP selects on a horizontally transmitted one and vice versa. Next, we present a fully coevolutionary model that examines the coevolutionarily stable states of both types of parasite in hosts with different characteristics.
Original languageEnglish
Pages (from-to)2408-2416
Number of pages9
JournalEvolution
Volume64
Issue number8
Early online date18 Mar 2010
DOIs
Publication statusPublished - Aug 2010

Fingerprint

parasite
Parasites
parasites
virulence
Virulence
Conflict (Psychology)
conflict
Feminization
Reproduction
feminization
vertical transmission
birth rate
Birth Rate
Sex Ratio

Keywords

  • evolution
  • feminization
  • life span
  • parasites
  • protection
  • vertical transmission
  • virulence

Cite this

The evolutionary implications of conflict between parasites with different transmission modes. / Jones, Edward Owen; White, Andrew; Boots, Michael.

In: Evolution, Vol. 64, No. 8, 08.2010, p. 2408-2416.

Research output: Contribution to journalArticle

Jones, Edward Owen ; White, Andrew ; Boots, Michael. / The evolutionary implications of conflict between parasites with different transmission modes. In: Evolution. 2010 ; Vol. 64, No. 8. pp. 2408-2416.
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abstract = "Understanding the processes that shape the evolution of parasites is a key challenge for evolutionary biology. It is well understood that different parasites may often infect the same host and that this may have important implications to the evolutionary behavior. Here we examine the evolutionary implications of the conflict that arises when two parasite species, one vertically transmitted and the other horizontally transmitted, infect the same host. We show that the presence of a vertically transmitted parasite (VTP) often leads to the evolution of higher virulence in horizontally transmitted parasites (HTPs), particularly if the VTPs are feminizing. The high virulence in some HTPs may therefore result from coinfection with cryptic VTPs. The impact of an HTP on a VTP evolution depends crucially on the nature of the life-history trade-offs. Fast virulent HTPs select for intermediate feminization and virulence in VTPs. Coevolutionary models show similar insights, but emphasize the importance of host life span to the outcome, with higher virulence in both types of parasite in short-lived hosts. Overall, our models emphasize the interplay of host and parasite characteristics in the evolutionary outcome and point the way for further empirical study. Host parasite theory often considers the impact of a single parasite on the dynamics of a single host. However, in natural systems hosts are often challenged by multiple parasites (Woolhouse et al. 2000; Haine et al. 2005; Woolhouse and Gowtage-Sequeria 2005) and this is of course likely to have important implications to the evolutionary dynamics of both parasites and hosts. For example, superinfection, where an invading strain displaces a resident strain in an individual host, often selects for more virulent and competitive parasites (Levin and Pimental 1981; Bremermann and Pickering 1983; Nowak and May 1994). If parasites coinfect the same individual, both within host and population level interactions become important, there are a range of outcomes resulting from multiple infections (Nowak and May 1994; van Baalen and Sabelis 1995; Brown et al. 2002) and in certain circumstances lead to the evolution of greater virulence and the possibility of parasite coexistence (Mosquera and Adler 1998). When parasites that share the same host have different transmission modes and in particular when there is vertically transmission from parent to offspring, conflicts arise. VTPs and horizontally transmitted parasites (HTPs) are both selected to minimize the additional mortality that infection causes. Reduced virulence benefits vertically transmitted parasites (VTPs) by extending the period of host reproduction from infected individuals and equally benefits HTPs by lengthening the infectious period. However, while the birth rate of the infected host is vital for the persistence and spread of a VTP, the fitness of HTPs is not directly affected by a change in host birth rate. Indeed, HTPs will be selected to castrate hosts if this leads to increased transmission (Jaenike 1996; O’Keefe and Antonovics 2002). Here, we examine, theoretically, the evolutionary implications of the resulting conflict over host reproduction between parasites with different transmission modes. Vertically transmitted parasites are particularly common in invertebrates (Werren 1997; Hogg et al. 2002; Kelly et al. 2003; Stouthamer et al. 2009) but are found across many taxa (Mims 1981). However, purely VTPs that cause virulence to their host will not persist without some other mechanism that compensates for this virulence (Fine 1975; Lipsitch et al. 1995). An important mechanism, by which a virulent VTP may persist, is the manipulation of the host's reproductive output through altering the sex ratio of the host by either increasing the total number of females born, converting males to females (feminization) or by male killing (Werren 1997; Kageyama et al. 2002; Cordaux et al. 2004; Zeh and Zeh 2006). Hurst (1993) showed, using theory that a sex-ratio distorting purely VTP can be maintained in a population even when there is selection against infected hosts by increasing the number of females born in each cohort. There is also evidence that some VTPs may protect the host against other natural enemies (Oliver et al. 2003; Haine et al. 2005). Recently, theory (Lively et al. 2005; Faeth et al. 2007; Jones et al. 2007) has shown that a purely VTP that causes some virulence to the host is able to persist by protecting the host from a virulent HTP. Furthermore, the greater the virulence of the HTP the easier for the vertical host to persist (Jones et al. 2007). Parasites that transmit vertically may also persist if they transmit to some extent horizontally (Busenburg et al. 1983; Regniere 1984) and in nature many pathogens may indeed possess both means of transmission (Burden et al. 2002; Hackett et al. 2005; Zhou et al. 2005). The evolutionary dynamics of parasites that possess both vertical and horizontal transmission modes have been examined in detail by Lipsitch et al. (1996). A key result is that as parasite numbers increase, they select for greater vertical transmission, due to both the higher potential for generation-to-generation infection and reduced encounters with susceptible individuals (Lipsitch et al. 1996). However, the evolutionary dynamics of purely HTPs and purely VTPs that coinfect the same hosts have not been considered in detail. 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T1 - The evolutionary implications of conflict between parasites with different transmission modes

AU - Jones, Edward Owen

AU - White, Andrew

AU - Boots, Michael

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N2 - Understanding the processes that shape the evolution of parasites is a key challenge for evolutionary biology. It is well understood that different parasites may often infect the same host and that this may have important implications to the evolutionary behavior. Here we examine the evolutionary implications of the conflict that arises when two parasite species, one vertically transmitted and the other horizontally transmitted, infect the same host. We show that the presence of a vertically transmitted parasite (VTP) often leads to the evolution of higher virulence in horizontally transmitted parasites (HTPs), particularly if the VTPs are feminizing. The high virulence in some HTPs may therefore result from coinfection with cryptic VTPs. The impact of an HTP on a VTP evolution depends crucially on the nature of the life-history trade-offs. Fast virulent HTPs select for intermediate feminization and virulence in VTPs. Coevolutionary models show similar insights, but emphasize the importance of host life span to the outcome, with higher virulence in both types of parasite in short-lived hosts. Overall, our models emphasize the interplay of host and parasite characteristics in the evolutionary outcome and point the way for further empirical study. Host parasite theory often considers the impact of a single parasite on the dynamics of a single host. However, in natural systems hosts are often challenged by multiple parasites (Woolhouse et al. 2000; Haine et al. 2005; Woolhouse and Gowtage-Sequeria 2005) and this is of course likely to have important implications to the evolutionary dynamics of both parasites and hosts. For example, superinfection, where an invading strain displaces a resident strain in an individual host, often selects for more virulent and competitive parasites (Levin and Pimental 1981; Bremermann and Pickering 1983; Nowak and May 1994). If parasites coinfect the same individual, both within host and population level interactions become important, there are a range of outcomes resulting from multiple infections (Nowak and May 1994; van Baalen and Sabelis 1995; Brown et al. 2002) and in certain circumstances lead to the evolution of greater virulence and the possibility of parasite coexistence (Mosquera and Adler 1998). When parasites that share the same host have different transmission modes and in particular when there is vertically transmission from parent to offspring, conflicts arise. VTPs and horizontally transmitted parasites (HTPs) are both selected to minimize the additional mortality that infection causes. Reduced virulence benefits vertically transmitted parasites (VTPs) by extending the period of host reproduction from infected individuals and equally benefits HTPs by lengthening the infectious period. However, while the birth rate of the infected host is vital for the persistence and spread of a VTP, the fitness of HTPs is not directly affected by a change in host birth rate. Indeed, HTPs will be selected to castrate hosts if this leads to increased transmission (Jaenike 1996; O’Keefe and Antonovics 2002). Here, we examine, theoretically, the evolutionary implications of the resulting conflict over host reproduction between parasites with different transmission modes. Vertically transmitted parasites are particularly common in invertebrates (Werren 1997; Hogg et al. 2002; Kelly et al. 2003; Stouthamer et al. 2009) but are found across many taxa (Mims 1981). However, purely VTPs that cause virulence to their host will not persist without some other mechanism that compensates for this virulence (Fine 1975; Lipsitch et al. 1995). An important mechanism, by which a virulent VTP may persist, is the manipulation of the host's reproductive output through altering the sex ratio of the host by either increasing the total number of females born, converting males to females (feminization) or by male killing (Werren 1997; Kageyama et al. 2002; Cordaux et al. 2004; Zeh and Zeh 2006). Hurst (1993) showed, using theory that a sex-ratio distorting purely VTP can be maintained in a population even when there is selection against infected hosts by increasing the number of females born in each cohort. There is also evidence that some VTPs may protect the host against other natural enemies (Oliver et al. 2003; Haine et al. 2005). Recently, theory (Lively et al. 2005; Faeth et al. 2007; Jones et al. 2007) has shown that a purely VTP that causes some virulence to the host is able to persist by protecting the host from a virulent HTP. Furthermore, the greater the virulence of the HTP the easier for the vertical host to persist (Jones et al. 2007). Parasites that transmit vertically may also persist if they transmit to some extent horizontally (Busenburg et al. 1983; Regniere 1984) and in nature many pathogens may indeed possess both means of transmission (Burden et al. 2002; Hackett et al. 2005; Zhou et al. 2005). The evolutionary dynamics of parasites that possess both vertical and horizontal transmission modes have been examined in detail by Lipsitch et al. (1996). A key result is that as parasite numbers increase, they select for greater vertical transmission, due to both the higher potential for generation-to-generation infection and reduced encounters with susceptible individuals (Lipsitch et al. 1996). However, the evolutionary dynamics of purely HTPs and purely VTPs that coinfect the same hosts have not been considered in detail. Here, our aim is to understand the evolutionary behavior of parasite pathogenicity arising from conflict between two different parasite species that can both infect the same host. We consider a purely VTP, maintained in populations through the manipulation of host reproduction, and assume that it coinfects with an HTP. We start with evolutionary models that examine how in turn the presence of a VTP selects on a horizontally transmitted one and vice versa. Next, we present a fully coevolutionary model that examines the coevolutionarily stable states of both types of parasite in hosts with different characteristics.

AB - Understanding the processes that shape the evolution of parasites is a key challenge for evolutionary biology. It is well understood that different parasites may often infect the same host and that this may have important implications to the evolutionary behavior. Here we examine the evolutionary implications of the conflict that arises when two parasite species, one vertically transmitted and the other horizontally transmitted, infect the same host. We show that the presence of a vertically transmitted parasite (VTP) often leads to the evolution of higher virulence in horizontally transmitted parasites (HTPs), particularly if the VTPs are feminizing. The high virulence in some HTPs may therefore result from coinfection with cryptic VTPs. The impact of an HTP on a VTP evolution depends crucially on the nature of the life-history trade-offs. Fast virulent HTPs select for intermediate feminization and virulence in VTPs. Coevolutionary models show similar insights, but emphasize the importance of host life span to the outcome, with higher virulence in both types of parasite in short-lived hosts. Overall, our models emphasize the interplay of host and parasite characteristics in the evolutionary outcome and point the way for further empirical study. Host parasite theory often considers the impact of a single parasite on the dynamics of a single host. However, in natural systems hosts are often challenged by multiple parasites (Woolhouse et al. 2000; Haine et al. 2005; Woolhouse and Gowtage-Sequeria 2005) and this is of course likely to have important implications to the evolutionary dynamics of both parasites and hosts. For example, superinfection, where an invading strain displaces a resident strain in an individual host, often selects for more virulent and competitive parasites (Levin and Pimental 1981; Bremermann and Pickering 1983; Nowak and May 1994). If parasites coinfect the same individual, both within host and population level interactions become important, there are a range of outcomes resulting from multiple infections (Nowak and May 1994; van Baalen and Sabelis 1995; Brown et al. 2002) and in certain circumstances lead to the evolution of greater virulence and the possibility of parasite coexistence (Mosquera and Adler 1998). When parasites that share the same host have different transmission modes and in particular when there is vertically transmission from parent to offspring, conflicts arise. VTPs and horizontally transmitted parasites (HTPs) are both selected to minimize the additional mortality that infection causes. Reduced virulence benefits vertically transmitted parasites (VTPs) by extending the period of host reproduction from infected individuals and equally benefits HTPs by lengthening the infectious period. However, while the birth rate of the infected host is vital for the persistence and spread of a VTP, the fitness of HTPs is not directly affected by a change in host birth rate. Indeed, HTPs will be selected to castrate hosts if this leads to increased transmission (Jaenike 1996; O’Keefe and Antonovics 2002). Here, we examine, theoretically, the evolutionary implications of the resulting conflict over host reproduction between parasites with different transmission modes. Vertically transmitted parasites are particularly common in invertebrates (Werren 1997; Hogg et al. 2002; Kelly et al. 2003; Stouthamer et al. 2009) but are found across many taxa (Mims 1981). However, purely VTPs that cause virulence to their host will not persist without some other mechanism that compensates for this virulence (Fine 1975; Lipsitch et al. 1995). An important mechanism, by which a virulent VTP may persist, is the manipulation of the host's reproductive output through altering the sex ratio of the host by either increasing the total number of females born, converting males to females (feminization) or by male killing (Werren 1997; Kageyama et al. 2002; Cordaux et al. 2004; Zeh and Zeh 2006). Hurst (1993) showed, using theory that a sex-ratio distorting purely VTP can be maintained in a population even when there is selection against infected hosts by increasing the number of females born in each cohort. There is also evidence that some VTPs may protect the host against other natural enemies (Oliver et al. 2003; Haine et al. 2005). Recently, theory (Lively et al. 2005; Faeth et al. 2007; Jones et al. 2007) has shown that a purely VTP that causes some virulence to the host is able to persist by protecting the host from a virulent HTP. Furthermore, the greater the virulence of the HTP the easier for the vertical host to persist (Jones et al. 2007). Parasites that transmit vertically may also persist if they transmit to some extent horizontally (Busenburg et al. 1983; Regniere 1984) and in nature many pathogens may indeed possess both means of transmission (Burden et al. 2002; Hackett et al. 2005; Zhou et al. 2005). The evolutionary dynamics of parasites that possess both vertical and horizontal transmission modes have been examined in detail by Lipsitch et al. (1996). A key result is that as parasite numbers increase, they select for greater vertical transmission, due to both the higher potential for generation-to-generation infection and reduced encounters with susceptible individuals (Lipsitch et al. 1996). However, the evolutionary dynamics of purely HTPs and purely VTPs that coinfect the same hosts have not been considered in detail. Here, our aim is to understand the evolutionary behavior of parasite pathogenicity arising from conflict between two different parasite species that can both infect the same host. We consider a purely VTP, maintained in populations through the manipulation of host reproduction, and assume that it coinfects with an HTP. We start with evolutionary models that examine how in turn the presence of a VTP selects on a horizontally transmitted one and vice versa. Next, we present a fully coevolutionary model that examines the coevolutionarily stable states of both types of parasite in hosts with different characteristics.

KW - evolution

KW - feminization

KW - life span

KW - parasites

KW - protection

KW - vertical transmission

KW - virulence

U2 - 10.1111/j.1558-5646.2010.00992.x

DO - 10.1111/j.1558-5646.2010.00992.x

M3 - Article

VL - 64

SP - 2408

EP - 2416

JO - Evolution

JF - Evolution

SN - 0014-3820

IS - 8

ER -