Fitness consequences of host colonization in two generalist fleas: Context-dependency and the effect of spatial co-occurrence.

We studied the fitness consequences of colonizing a novel host by experimental lines of fleas (Synosternus cleopatrae and Xenopsylla ramesis) maintained for 18-22 generations on the principal or novel (sympatric or allopatric) hosts via number, developmental success and size of the offspring of the fleas exploiting these hosts. We asked whether (a) fitness on non-principal hosts increases after prolonged maintenance; (b) the colonization success depends on the spatial co-occurrence of a flea and a host and (c) colonization of a novel host is accompanied by a decreased ability to exploit an original host. The ability of fleas to colonize novel hosts differed between species, with S. cleopatrae, but not X. ramesis, increasing its offspring production on novel hosts. Spatial co-occurrence did not affect colonization success. Maintenance on an alternative host was not accompanied by decreased adaptation to the original host. When fleas returned to the original host, their reproductive output was higher than that of their ancestors. We conclude that the success of colonizing a novel host is (a) context-dependent and varies between flea and host species and (b) not accompanied by the loss of ability to exploit an ancestral host but may lead to an increase in this ability.

Adaptation to a novel host and performance trade-off in host-generalist and host-specific insect ectoparasites.

We investigated the performance trade-offs of fleas (Siphonaptera) while adapting to a novel host using two host generalists (Xenopsylla conformis and Xenopsylla ramesis) and one host specialist (Parapulex chephrenis) maintained on their principal hosts (Meriones crassus for Xenopsylla and Acomys cahirinus for P. chephrenis). We asked whether, over generations, (i) a host generalist may become a specialist by evolving the ability to exploit a novel host and losing the ability to exploit an original host and (ii) a host specialist can become a generalist by evolving the ability to exploit a novel host without losing the ability to exploit an original host. We established an experimental line of each species on a novel host (Acomys russatus for Xenopsylla and M. crassus for P. chephrenis) and maintained this line on this host during 23 generations. We compared reproductive performance of progenitors of each line and their descendants when they exploited either original or novel host in terms of egg number and size, hatching success, offspring production, and offspring size. We found changes in performance over generations in female offspring size only. Xenopsylla conformis demonstrated a tendency to become a host specialist (increased performance on the novel host with a concomitant decreased performance on the original host), whereas P. chephrenis demonstrated a tendency to become a host generalist (increased performance on the novel host without a concomitant decreased performance on the original host). We conclude that the probability of generalist to specialist transition, and vice versa, is context-dependent and varies between species.

Colonization of a novel host by fleas: changes in egg production and egg size.

We studied the success of fleas, Synosternus cleopatrae and Xenopsylla ramesis, in switching to a novel host by establishing experimental lines maintained on different hosts for 18 generations. Fleas fed on principal (P-line) or novel hosts, either sympatric with (S-line) or allopatric to (A-line) a flea and its principal host, then we assessed their reproductive performance via the number and size of eggs. We compared reproductive performance between hosts within a line and between lines within a host asking: (a) whether fleas adapt to a novel host species after multiple generations; (b) if yes, whether the pattern of adaptation differs between novel host species sympatric with or allopatric to a flea and its principal host; and (c) adaptation to a novel host is accompanied with a loss of success in exploitation of an original host. Fleas from the S- and A-lines increased their egg production on a novel host (except X. ramesis from the S-line). S. cleopatrae from the S-line but not the A-line increased egg size on a novel host, whereas X. ramesis from the A-line but not the S-line produced larger eggs from a novel host. We found no indication of a loss of reproductive performance on the original host while adapting to a novel host. We conclude that fleas are able to switch rapidly to a new host with the pattern of a switch to either sympatric or an allopatric host depending on the identities of both flea and host species.