How relaxed preferences facilitate the evolution of novel animal signals

The evolution of novel animal signals is critical to the generation of
biodiversity. Here, we explore how new sexual signals become established.
This process is challenging to explain because if receiver preferences are
coupled with existing signals, then most receivers should discriminate
against new signals. We investigated an underappreciated hypothesis:
relaxed receiver preferences facilitate novel signal evolution by allowing
new signals to establish a foothold. Further, we probed the mechanistic
underpinnings of relaxed preferences by combining field-based and common
garden approaches, allowing us to investigate evolution and plasticity as
mechanisms. We capitalized on the Pacific field cricket, Teleogryllus
oceanicus, a species that has recently evolved multiple novel acoustic
signals (e.g., purring and rattling) in response to an eavesdropping
parasitoid fly only found in the crickets’ introduced range in Hawaii. To
test the hypothesis that selection associated with high search costs in
introduced populations leads to relaxed mating preferences and determine
whether such relaxation is plastic, we conducted sound preference
(phonotaxis) trials with females from the cricket’s native range
(Australia and French Polynesia, where the fly is absent) and its
introduced range (Hawaii, where the fly is present). We presented females
with novel songs plus the typical, ancestral song. Differences in
phonotactic behavior between the lab and field settings would indicate
plasticity in preferences. Using Generalized Linear Mixed Models (GLMM)
with whether the female cricket was phonotactic to a song (y/n) as a
response variable, we found that Australian and French Polynesian females
were quite plastic; they discriminated strongly against most songs in the
field, but were much more phonotactic to rattling and the typical song in
the lab. However, Hawaiian females exhibited little plasticity and were
consistently highly responsive to the rattling and typical songs in the
lab and field. This pattern points to a loss of ancestral plasticity in
female preferences sometime after colonizing Hawaii, resulting in
heightened responsiveness to all songs, allowing novel signals to
establish. We then asked which specific preference function traits
(tolerance, strength, and/or responsiveness) differed among regions to
better understand what is ‘relaxed’ about preferences in Hawaii by
generating individual and region-level preference functions for females
from each region with respect to the purring, rattling, and ancestral
stimuli. When examining whether females were phonotactic or not and how
quickly they contacted stimuli, responsiveness, tolerance, and preference
strength differed among regions. Finally, we developed a
computational model to estimate the distances at which female T. oceancius
from Australia and French Polynesia should be able to hear and use the
purring, rattling, and typical calling songs. A model of mean
peak frequencies and amplitudes among each song type revealed dramatic
differences in effective hearing distances across song types. Our results
provide insight into how novel signals gain a foothold when they initially
invade, after which coupled preferences may eventually evolve, perhaps
leading to reproductive isolation. Alternatively, relaxed preferences may
remain longer term, facilitating the maintenance of signal diversity
within populations.