The shapes and the colors: distinct sexual traits among tube blennies reflect a multi-layered selection scenario.

The “survival of the fittest”. The common theme that surrounds our general understanding of evolution and natural selection is that the organisms that are better adapted to a certain environment have a higher chance of surviving/reproducing. That is a concept that proves to be intuitive at a certain level, if an organism presents more “favourable”, “efficient” traits, they tend to be better competitors. Pretty straight-forward? Sure, but sometimes it is not the case. Darwin is most known for his insights on natural selection, however the same Darwin was also intrigued and fascinated by another kind of selection, sometimes left in the shade of its more famous sibling: Sexual selection.

Darwin (1871) draws the attention to how males and females of the same species can look very different (sexual dimorphism), sometimes manifesting morphological attributes or behaviours that at a first glance are odd, energetically expensive and disadvantageous to survival. Considering that the most “efficient” combination of traits is the best one, that creates a bit of contradiction. Think about the exuberant feathers from a sexually active peacock or the over-developed antlers in deer. Features like these have a clear purpose: reproduction. And reproduction is key to fitness and, of course, the evolutionary success of a group. However, how does this dimorphism evolve? What is the evolutionary relationship (phylogenetic) significance of these characters?

A recently published study by Hastings uses a group of marine tropical fishes, the tube blennies (check them out here)   to investigate the degree of sexual dimorphism between species of the family Chaenopsidae (sensu Lin & Hastings, 2011) and the evolutionary patterns of these features from a phylogenetic perspective. What makes this group particularly interesting for this kind of study is that within them, some species are monomorphic, some are “somewhat dimorphic” and some are clearly dimorphic (Stephens 1963, 1970; Hastings 1991, 2002). From their characteristic habitats (vacant tests of invertebrates, like barnacles, mollusk shells and polychaete tubes), male tube blennies display and court female counterparts by extending outside their shelters, erecting their dorsal fins and partially retreating back in. Females generally prefer larger males and males defending higher quality shelters, a resource that is responsible for intense male-male competition.

Hastings compiled an extensive list of dimorphic characters, including osteological, morphometrical, anatomical, coloration and even sensorial ones, and analyzed the patterns of sexual dimorphism over a compilation of recent published phylogenies for tube blennies. He found out that osteological characters in the head region, are usually more ossified in males when compared to females. Soft anatomy also varies between males and females (also in the head region), but are not exclusive to males this time. The shape and size of anterior dorsal fins are also evident dimorphic characters. Regarding colour patterns, males usually have denser melanophores than females, especially during breeding season, mostly in the head and anterior portion of the body of the fish. This is the region that is most visible in both aggressive and courtship displays

One of the key findings is that sexual dimorphism is not uniformly distributed among chaenopsids, meaning that dimorphism has appeared in this group more than once during their evolutionary history. Not only the patterns observed are independent among distinct tube blenny species, they also change in intensity between genera and species: some being moderate, as observed in the genus Chaenopsis, or some more evident, like in Emblemaria. In addition evolution has occurred in males, as predicted by sexual selection theory, but also independently in females.  Hastings hypothesizes that the observed variation is due in part to differences in microhabitats occupied by males and females of different species. These differences are fundamental in understanding the selective pressures over distinct chaenopsids, because these habitats are fundamental to their survival and reproduction. But habitat does not seem to be the only factor involved in the observed dimorphism. On top of competition, epigamic selection (being attractive to the opposite sex) also plays a major role (Anderson 1984; Prum, 2017).

Tube blennies are one of many fishes that have developed complex sexual behaviours through-out their evolutionary history. The complexity observed at a phylogenetic level, for example the occurrence of reversal/losses of traits (Omland, 1997; Weins 2001) and divergence in females and males, requires more complete and in depth studies treating males and females independently to properly address the real life history of many fish groups, and in special the Chaenopsidae.

AUTHOR

J.P. (short for João Pedro) Fontenelle is a PhD candidate at the University of Toronto Scarborough. After getting a MSc. in zoology from the University of São Paulo, he decided to dive in the world of ecology and evolution by studying phylogenetics and biogeography of Neotropical fishes. His work focus on diversification at different time scales, taking into account on how ecological gradients can affect the evolution of different groups and how a combination of molecular and morphological methodologies can be used to explore such questions. Twitter: @jpf_ishes / Researchgate: https://www.researchgate.net/profile/Joao_Pedro_Fontenelle

References:

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Hastings PA. 1991a. The ontogeny of sexual dimorphism in Coralliozetus angelica (Chaenopsidae). Copeia 1991:969–78

Hastings PA. 2002. Evolution of morphological and behavioral ontogenies in females of a highly dimorphic clade of blennioid fishes. Evolution 56:1644–54.

Lin HC, Hastings PA. 2011. Evolution of a Neotropical marine fish lineage (subfamily Chaenopsinae, suborder Blennioidei) based on phylogenetic analysis of combined molecular and morphological data. Mol Phylogenet Evol 60: 236–48.

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