Host selection and ovipositor length in eight sympatric species of sculpins that deposit their eggs into tunicates or sponges

Abstract

Interspecific interactions between parasites and hosts can influence the evolution of behavioural and morphological adaptations of both parasites and their hosts. There is, however, little empirical evidence available regarding the evolution of reproductive traits driven by these interactions. In this paper, we investigated host selection and ovipositor length in nine sympatric marine sculpins that oviposit into tunicates or sponges. Field and genetic studies have revealed host use for eight out of nine species of sculpins investigated here: five species of Pseudoblennius, two species of Furcina and one species of Vellitor. For one species studied (V. minutus), no egg masses could be found. Ovipositor length reflects morphology of host species utilised: six sculpin species had extremely long ovipositors allowing females to attach eggs to the deep atrium of solitary tunicates, whereas the two species that attached their eggs to the small space of atrial siphon of colonial tunicates and the spongocoel of sponges had short ovipositors. Ovipositor length varied between solitary-tunicate spawners and species with longer ovipositors selected larger tunicates. Since the ancestral form is non-parasitic, the ovipositor evolved as an adaptation to utilise sponges and tunicates as hosts. Sculpins found sympatrically may show host specificity to avoid interspecific competition for spawning niches and ovipositors may have evolved depending on the species and size of host invertebrates.

First Description of Reproductive Behavior and Alternative Reproductive Strategy in the Deep-sea Fish, Careproctus pellucidus.

“…However, the process, procedure, and prior behaviors of reproduction (e.g., territoriality, intra-and intersexual selection, courtship, and spawning behavior), which are key to understanding the adaptive signi cance and evolutionary background of reproductive strategies in the deep-sea environment, have not been observed. From another point of view, it is expected that the dispersion of spawning substrate utilization makes the species with similar spawning niches less di cult to live sympatrically because it reduces interspeci c competition (Reichard et al 2007;Awata et al 2019). There is a possibility that the unique preference for the spawning substrate in snail shes has a similar function to the above.…”

The first record of egg masses in tunicates deposited by the snubnose sculpin, Orthonopias triacis, from the Northeastern Pacific: evidence for convergent evolution of an unusual reproductive strategy

“…Among marine fishes, host invertebrates used by ostracophilous fishes are diverse. Blennies, marine sculpins, sea ravens, poachers and snailfishes oviposit in the spongocoels of sponges (Busby et al, 2012;Chernova, 2014;Karplus, 2014;Momota & Munehara, 2017) and in the branchial chambers of crabs (e.g., Gardner et al, 2016;Hunter, 1969;Matsuzaki et al, 2020;Poltev & Mukhametov, 2009), whereas the Japanese tubesnout Aulichthys japonicus Brevoort, 1862 (Akagawa et al, 2008) and marine sculpins (Awata et al, 2019;Goto & Oba, 2019;Nishida et al, 2008) oviposit in the atria of tunicates. As has been found in freshwater bitterlings, ostracophilous snailfishes and sculpins have elongated ovipositors (Awata et al, 2019;Hunter, 1969).…”

“…The marine sculpins (Psychrolutidae, 64 genera, 214 species) and sea ravens and poachers (Agonidae, 25 genera 59 species), that belong to the Infraorder Cottales (Betancur-R et al, 2017;Nelson et al, 2016;Smith & Busby, 2014), represent a diverse group exhibiting morphological variation associated with specific reproductive strategies (Abe & Munehara, 2009;Buser et al, 2017;Knope, 2013;Koya et al, 2011). They represent an ideal system to study morphological and behavioural adaptations driven by the interactions between parasites and hosts because several sculpins, sea ravens and poachers are known to parasitize live invertebrates for egg deposition (Abe & Munehara, 2009;Busby et al, 2012;Karplus, 2014;Momota & Munehara, 2017), and a recent study has shown that ostracophilous marine sculpins exhibit interspecific variation in host selection and female reproductive traits such as ovipositor length (Awata et al, 2019). There are three patterns of host use by ovipositing sculpins including species that primarily use colonial tunicates, those that exclusively use solitary tunicates and those that use exclusively sponges (Awata et al, 2019), showing host specificity.…”

“…They represent an ideal system to study morphological and behavioural adaptations driven by the interactions between parasites and hosts because several sculpins, sea ravens and poachers are known to parasitize live invertebrates for egg deposition (Abe & Munehara, 2009;Busby et al, 2012;Karplus, 2014;Momota & Munehara, 2017), and a recent study has shown that ostracophilous marine sculpins exhibit interspecific variation in host selection and female reproductive traits such as ovipositor length (Awata et al, 2019). There are three patterns of host use by ovipositing sculpins including species that primarily use colonial tunicates, those that exclusively use solitary tunicates and those that use exclusively sponges (Awata et al, 2019), showing host specificity. Furthermore, species that occur in sympatry use different host species (e.g., tunicates or sponges) with different host sizes.…”

“…Furthermore, species that occur in sympatry use different host species (e.g., tunicates or sponges) with different host sizes. The authors of this study proposed that ovipositor length may have co-evolved to accommodate morphology of specific host invertebrates (Awata et al, 2019). Indeed, the ovipositor of species using solitary tunicates as hosts (four species of the genus Pseudoblennius and two species of the genus Furcina) is much longer than species using colonial tunicates and/or sponges [Pseudoblennius marmoratus (Döderlein, 1884) and Vellitor centropomus (Richardson, 1850): Awata et al, 2019].…”