Regressive evolution of the arthropod tritocerebral segment linked to functional divergence of the Hox genelabial

Abstract

The intercalary segment is a limbless version of the tritocerebral segment and is present in the head of all insects, whereas other extant arthropods have retained limbs on their tritocerebral segment (e.g. the pedipalp limbs in spiders). The evolutionary origin of limb loss on the intercalary segment has puzzled zoologists for over a century. Here we show that an intercalary segment-like phenotype can be created in spiders by interfering with the function of the Hox gene labial. This links the origin of the intercalary segment to a functional change in labial. We show that in the spider Parasteatoda tepidariorum the labial gene has two functions: one function in head tissue maintenance that is conserved between spiders and insects, and a second function in pedipalp limb promotion and specification, which is only present in spiders. These results imply that labial was originally crucial for limb formation on the tritocerebral segment, but that it has lost this particular subfunction in the insect ancestor, resulting in limb loss on the intercalary segment. Such loss of a subfunction is a way to avoid adverse pleiotropic effects normally associated with mutations in developmental genes, and may thus be a common mechanism to accelerate regressive evolution.

The evolution of selector gene function: Expression dynamics and regulatory interactions of tiptop/teashirt across Arthropoda

“…In addition, whereas trunk Hox genes like Antp and Ubx maintain tsh expression in the posterior compartment of specific D. melanogaster trunk segments, homologs of neither of these genes are expressed in the prosoma of arachnids during stages corresponding to leg fate specification (Khadjeh et al, ; Schwager et al, ; Sharma et al, ; Sharma, Schwager, Extavour, & Wheeler, ). Furthermore, the limited data available on Hox gene function in arachnids (e.g., lab‐ 1, Dfd‐1 , Antp‐1 ), in addition to expression patterns of centipede posterior Hox genes in the posterior trunk (the region correspond to the appendage‐free insect abdomen), have shown that orthology of Hox genes does not correspond to homology of function between insects, centipedes, and arachnids (Hughes & Kaufman, ; Khadjeh et al, ; Pechmann et al, ). The evolution of tio/tsh and Hox expression domains thus appears to be decoupled.…”

“…The proximo‐distal axis of panarthropod appendages in particular is patterned by a suite of transcription factors whose positional relationships are broadly conserved (Abu‐Shaar & Mann, ; Cohen, Brönner, Küttner, Jürgens, & Jäckle, ; Dong, Chu, & Panganiban, ; Dong, Dicks, & Panganiban, ; Janssen, Eriksson, Budd, Akam, & Prpic, ; Mardon, Solomon, & Rubin, ; Panganiban et al, ; Panganiban, Nagy, & Carroll, ; Panganiban, Sebring, Nagy, & Carroll, ; Prpic, Janssen, Wigand, Klingler, & Damen, ; Schoppmeier & Damen, ; Sharma, Schwager, Extavour, & Giribet, ). Similarly, the establishment of arthropod appendage types along the antero‐posterior axis is achieved by the activity of trunk Hox genes throughout the phylum (Emerald & Cohen, ; Liubicich et al, ; Martin et al, ; Pavlopoulos et al, ; Pechmann, Schwager, Turetzek, & Prpic, ; Struhl, ; Struhl & White, ) and homothorax (Casares & Mann, ; Ronco et al, ; Sharma et al, ).…”

six3 acts upstream of foxQ2 in labrum and neural development in the spider Parasteatoda tepidariorum

“…Large-scale duplication of genes in spiders has been reported in P. tepidariorum before (Pechmann et al 2015;Schomburg et al 2015;Schwager et al 2017;Leite et al 2018). Therefore, we wanted to identify the total number of foxQ2 orthologs in P. tepidariorum.…”

The house spider genome reveals an ancient whole-genome duplication during arachnid evolution

“…lab-1 expression (Akiyama- Oda and Oda, 2010;Pechmann et al, 2015) appears much later in development than lab-2 (Pechmann et al, 2009), at stage 4 compared to stage 6 ( Fig. 9).…”

“…(e.g. lab, Scr, Ubx and AbdA) (Akiyama-Oda and Oda, 2010;Pechmann et al, 2015) (Fig. 9B-G), ifnot 15 to 20 hours (pb, Dfd, Antp), and even 30 hours in the case of AbdB(Fig 9A, H-M).…”