Exaggerated male forelegs are not more differentiated than wing morphology in two widespread sister species of black scavenger flies

Abstract

Sexual selection represents a potent force that can drive rapid population differentiation in traits related to reproductive success. Hence, sexual traits are expected to show greater population divergence than non‐sexual traits. We test this prediction by exploring patterns of morphological differentiation of the exaggerated fore femur (a male‐specific sexual trait) and the wing (a non‐sexual trait) among allopatric and sympatric populations of the widespread sister dung fly species Sepsis neocynipsea and Sepsis cynipsea (Diptera: Sepsidae). While both species occur in Eurasia, S. neocynipsea also abounds in North America, albeit previous studies suggest strong differentiation in morphology, behavior, and mating systems. To evaluate the degree of differentiation expected under neutrality between S. cynipsea, European S. neocynipsea, and North American S. neocynipsea, we genotyped 30 populations at nine microsatellite markers, revealing almost equal differentiation between and minor differentiation among geographic populations within the three lineages. Landmark‐based analysis of 18 populations reared at constant 18 and 24°C in a laboratory common garden revealed moderate temperature‐dependent phenotypic plasticity and significant heritable differentiation in size and shape of male forelegs and wings among iso‐female lines of the three lineages. Following the biological species concept, there was weaker differentiation between cross‐continental populations of S. neocynipsea relative to S. cynipsea, and more fore femur differentiation between the two species in sympatry versus allopatry (presumably due to character displacement). Contrary to expectation, wing morphology showed as much shape differentiation between evolutionary independent lineages as fore femora, providing no evidence for faster diversification of traits primarily engaged in mating.

Sexual size dimorphism is associated with reproductive life history trait differentiation in coexisting sepsid flies

“…Multiple widespread species with apparently very similar ecological niches coexist in Europe, and all 12 Sepsis species occurring in Switzerland may be found on the same pasture (Rohner et al 2014(Rohner et al , 2015(Rohner et al , 2019. Sepsids have received considerable attention in behavioral ecology and evolutionary research because of their diverse mating systems (Eberhard 2001a(Eberhard , 2003Kraushaar and Blanckenhorn 2002;Mühlhäuser and Blanckenhorn 2002;Martin and Hosken 2004;Tan et al 2011;Puniamoorthy 2014; and extraordinary secondary sexual morphology of forelegs and convergently evolved abdominal appendages ( Eberhard 2001b;Bowsher and Nijhout 2009;Bowsher et al 2013;Herath et al 2015;Baur et al 2019Baur et al , 2020. Mating systems range from species with classic female choice and scramble competition to systems with pronounced male competition (cf.…”

Intraspecific mating system evolution and its effect on complex male secondary sexual traits: Does male–male competition increase selection on size or shape?

“…Surprisingly, however, this was also the case for wing size and shape, a trait assumed to be primarily under natural selection (e.g. in drosophilids: Gilchrist et al, , but also in sepsids: Baur et al, ; Rohner et al, 2019; Rohner et al, ). Yet, after accounting for allometric scaling, we found little evidence for direct precopulatory sexual selection on fore femur (or wing) morphology beyond the documented selection on overall body size (Puniamoorthy, Schafer, et al, ; Rohner et al, ; this study).…”

“…Surprisingly, however, this was also the case for wing size and shape, a trait assumed to be primarily under natural selection (e.g. in drosophilids: Gilchrist et al, 2000, but also in sepsids: Baur et al, 2019;Rohner et al, 2019;Rohner et al, 2015). Yet, after accounting for allometric scaling, we found little evidence for direct precopulatory sexual selection on fore femur (or wing) morphology beyond the documented selection on overall body size (Puniamoorthy, Schafer, et al, 2012b; Rohner TA B L E 3 Procrustes distance between mean shape before and after selection, the norm of the selection differential (||S||), as well as the significance of the two-block PLS analyses for femur morphology by species, direction of SSD and operational sex ratio (OSR).…”

“…abdominal sternite brushes, pronounced fore leg modifications: Eberhard, 2001aEberhard, , 2001bEberhard, , 2005 and mating behaviour (Puniamoorthy, 2014;Puniamoorthy, Su, & Meier, 2008). Such differentiation is however not limited to the species level but can also be found within species (Baur, Giesen, Rohner, Blanckenhorn, & Schäfer, 2019). Populations of some widespread species exhibit clear differences in mating systems.…”

Evolutionary origins of sexual dimorphism : Lessons from female-limited mimicry in butterflies.

“…Similarly, costly exaggerated trait in males may be regarded as a results of sexual conflicts: female prefer this expensive trait sign of mate quality (handicap principle [Zahavi, 1975]) leading to maladaptive trait disfavoured by natural selection [Johnstone, 1995]. In black scavenger flies Sepsis cynipsea and Sepsis neocynipsea species differentiation of exaggerated male forelegs is higher in sympatric population [Baur et al, 2020], suggesting than species interactions may indeed be a key evolutionary force involved in the evolution of exaggerated trait in males.…”