Study of the phenotypic diversity and evolutionary history of goatfishes (Teleostei, Mullidae)

Goatfishes (Mullidae) are a family of demersal fishes widely distributed across the globe, particularly
in tropical and subtropical regions. They are recognized as one of the major families associated with
coral reefs, alongside Pomacentridae, Acanthuridae, Labridae, and Chaetodontidae, but Mullidae stand
out due to several unique characteristics. Unlike dominant reef families that mainly exploit the reef
structure, Mullidae also widely occupy adjacent habitats such as sandy areas, seagrass beds, or
mangroves. Primarily benthic carnivores, they capture small prey buried in the substrate using a pair of
hyoid barbels located under the chin. This sensory structure, covered by taste buds, is unique among
reef fishes. Furthermore, while most reef fish families emerged 50 to 60 million years ago, Mullidae
appeared more recently, around 25 million years ago. They are notably absent from Eocene deposits
where the majority of reef fish were already present.
The aim of this doctoral thesis is to better understand the evolutionary processes behind the diversity of
tropical coastal fishes, using Mullidae as a model group. To do so, I built a robust phylogenomic tree
including 78% of described species, based on thousands of loci obtained through the ultraconserved
elements (UCEs) method. I also assembled a phenotypic dataset covering various aspects of Mullidae
ecology such as general body shape, head shape, anatomical characteristics of barbels, and pigmentation
patterns. Additionally, ecological data were collected during a case study in Madagascar, including
stomach content and stable isotope analyses. All these data were analyzed within an integrative
phylogenetic framework to describe the diversification of Mullidae, particularly by testing three possible
evolutionary scenarios: adaptive radiation, non-adaptive radiation, and multiple evolutionary
convergences.
The study of an assemblage of fourteen Mullidae species from the Grand Récif of Toliara (Madagascar)
revealed a strong link between head shape and trophic ecology. In particular, snout length and eye size
and position were directly associated with distinct feeding strategies. Species of the Upeneus genus,
characterized by a short snout and a large, anteriorly positioned eye, forage through the upper substrate
layers using their snout. In contrast, species of the Parupeneus genus, with an elongated snout and
smaller, more posterior eyes, exploit reef crevices or deeper sediment layers. Isotopic analysis revealed
trophic segregation organized along a spatial gradient from the lagoon to the outer reef slope. The
distribution of Parupeneus species is directly linked to head shape: long-snouted species are found on
the outer reef slope, while short-snouted species mainly inhabit the lagoon. Upeneus occurs exclusively
on the outer slope, whereas Mulloidichthys appears to occupy or migrate between both zones. The
morphological analysis of barbels also highlighted the singularity of the genus Upeneus, which displays
shorter barbels but with a higher density of small taste buds, opposite to Parupeneus and Mulloidichthys.
This barbel morphological variation is likely associated with different prey-searching strategies,
especially between various substrate types (i.e., reef vs soft substrate).
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The new phylogenomic tree, including 76 species, refines interspecific relationships while confirming
the monophyly of the six genera and two distinct subgroups within the Upeneus genus. The exploration
of lineage accumulation dynamics over time revealed a residual signal of elevated early speciation rates
followed by a progressive decline. This speciation dynamic appears to have been accompanied by a very
low extinction rate.
The study of the diversification of different phenotypic traits (general body morphology, head shape,
barbel characteristics, and pigmentation patterns) revealed contrasting evolutionary patterns among
traits. Divergences in head shape among lineages emerged early in Mullidae evolutionary history and
remained relatively stable. Pigmentation patterns diverged later within genera and showed numerous
convergences. Barbel characteristics were highly conserved across genera, with the exception of a recent
diversification within Upeneus. General body morphology evolved rather constantly over time.
All of these results support a scenario of adaptive radiation likely initiated by the emergence of a key
innovation represented by the hyoid barbels and unfolding in several phases. A first diversification phase
would be linked to distinct foraging strategies associated with head shape variation. Then, lineages
would have diversified through the use of different foraging zones. Finally, differentiation in
pigmentation patterns would be associated with divergence in visual signaling. Although Mullidae differ
from the dominant reef fish families in their evolutionary and ecological characteristics, the evidence of
adaptive radiation in this group echoes other similar examples in dominant reef taxa such as clownfishes
or triggerfishes. However, the stepwise progression of this radiation—rarely documented among major
families—has so far only been observed in parrotfishes. This highlights that the immense diversity of
reef ichthyofauna has been shaped by an equally vast and nuanced diversity of evolutionary processes.