Modelling the spread and connectivity of waterborne marine pathogens: the case of PaV1 in the Caribbean

Abstract

The PaV1 virus infects spiny lobsters (Panulirus argus) throughout most of the Caribbean, where its prevalence in adult lobsters can reach 17% and where it poses a significant risk of mortality for juveniles. Recent studies indicate that vertical transmission of the virus is unlikely and PaV1 has not been identified in the phyllosoma larval stages. Yet, the pathogen appears subclinically in post-larvae collected near the coast, suggesting that lobster post-larvae may harbour the virus and perhaps have aided in the dispersal of the pathogen. Laboratory and field experiments also confirm the waterborne transmission of the virus to post-larval and early benthic juvenile stages, but its viability in the water column may be limited to a few days. Here, we coupled Lagrangian modelling with a flexible matrix model of waterborne and post-larval-based pathogen dispersal in the Caribbean to investigate how a large area with complex hydrology influences the theoretical spread of disease. Our results indicate that if the virus is waterborne and only viable for a few days, then it is unlikely to impact both the Eastern and Northwestern Caribbean, which are separated by dispersal barriers. However, if PaV1 can be transported between locations by infected post-larvae, then the entire Caribbean becomes linked by pathogen dispersal with higher viral prevalence in the North. We identify possible regions from which pathogens are most likely to spread, and highlight Caribbean locations that function as dispersal "gateways" that could facilitate the rapid spread of pathogens into otherwise isolated areas.

Panulirus argus virus 1 detected in oceanic postlarvae of Caribbean spiny lobster: implications for disease dispersal

“…Our analyses showed that PaV1 from infected puerulus 2 shared greater homology with PaV1 sequences obtained from lobsters from Puerto Rico than with those from Mexico (including the infected lobster used as a positive control) and Florida, suggesting high gene flow and long-distance dispersal (Moss et al 2013) and providing evidence that postlarvae can act as a vector for PaV1 dispersal across the wider Caribbean region, as recently modeled by Kough et al (2015). Whether postlarvae infected offshore act as asymptomatic carriers of PaV1 into the settlement habitats, as do shrimp postlarvae infected with white spot syndrome virus (Thakur et al 2002), or develop the disease after molting into benthic juveniles warrants further evaluation.…”

“…), suggesting that pueruli acquire PaV1 from the water. Results from a recent modeling approach (Kough et al 2015) revealed that if PaV1 is transported by infected postlarvae rather than through water alone, then the results of the model would be more consistent with genetic linkages of PaV1 as reported by Moss et al (2013).…”

“…This would suggest that the infected postlarvae acquired PaV1 in offshore waters, because after metamorphosis, the movement of pueruli is directed shoreward rather than being dispersed at random or by prevailing currents (Phillips et al 2006). Although there is limited information on how long PaV1 virions can stay infective outside the hosts in natural seawater (Kough et al 2015), some viral diseases in marine systems have undergone unusually rapid propagation, suggesting a lack of barriers to dispersal in some parts of the ocean and the potential for long-term survival outside their hosts (McCallum et al 2003). Marine aggregates, onto which viruses may adsorb, can protect viruses from various sources of inactivation and provide them with a means for horizontal transport, potentially resulting in increased infection of organisms such as zooplankton (Wein bauer et al 2009).…”

The influence of spawning periodicity on population connectivity

“…After resolving conflicts between real-world spatial data and the land mask of the hydrodynamic models, we obtained 1682 coral reef habitat locations (Kough et al 2014;ESM Fig. 2).…”

The relevance of larval biology on spatiotemporal patterns of pathogen connectivity among open-marine salmon farms

“…Population scale/epidemiological studies often use sea-way distance as a proxy for circulation (Aldrin et al 2013; Rees et al 2015). Studies that have explicitly modeled regional circulation (Stucchi et al 2011;Adams et al 2012;Asplin et al 2014;Kough et al 2015;Johnsen et al 2016;Kragesteen et al 2017;Salama et al 2017;Samsing et al 2017) typically do not elucidate the contributions of individual drivers to infectious pressure experienced by potential hosts.…”